Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 [email protected] [email protected] or [email protected] 320 E-mail: 35805. VP-62, AL Huntsville, Center/NASA, Laboratory, Astrobiology Technology Dr., Sparkman and Sciences Space National this the of support and for research. Astromaterials Fund in Discretionary Biomarkers for Director’s Center NASA/JSC Center NASA/MSFC the and ols al hrh igna USA Virginia, Church, Falls Noblis, Tang Jane Huntsville, Laboratory, USA Astrobiology Alabama, Center/NASA, Technology and Sciences Hoover Space B. National Richard and Pikuta V. Elena Life of Limits the at Extremophiles Microbial Copyright Microbiology, in Reviews Critical oa hscletee VndnBr 03.Lf naisall inhabits Life 2003). Burg den (Van extremes physical referred as are to that radiation and pressure, as temperature, extremes, to geochemical opposed as considered Tradition- are salinity environment. and our pH ally, composing factors biological formed. physicochemical and been of variety have broad the ecosystems by differ of ecosystems These number a changes, climatic INTRODUCTION Keywords irfsisi eertsi h otx ftesgicneo mi- of significance of the studies Astrobiology. of recent to context extremophiles review the crobial briefly in and meteorites soils, in from microfossils as extremophiles extremophiles such microbial of of finding places of species the unusual fields different discuss for all also life We in of extremophiles. studies limits the of summarize status we and review current this the In extreme-groups. could show several organism of one ac- characteristics since multiple unite factors the environmental reflect different radioresistant of cannot tions systematics and aci- artificial psychrophilic, barophilic, This thermophilic, species. halophilic, of: alkaliphilic, composed is dophilic, it physico-chemical modern of and result, framework factors, a a As in environments. formed extreme diversity of prokaryotic spectrum geological wide adapt of a to life to genesis allowed probably genome the the known of currently for Flexibility all ecosystems. of responsible creation and are evolution the during they structures and Earth on O:10.1080/10408410701451948 DOI: online 1549-7828 / print 1040-841X ISSN: uigErhseouin copne ygohscland geophysical by accompanied evolution, Earth’s During rkroi xrmpie eetefis ersnaie flife of representatives first the were extremophiles Prokaryotic drs orsodnet ln .Pkt,RcadB Hoover B. Richard Pikuta, V. Elena to comments correspondence helpful Address their for reviewers the thank to 2007. want May 10 We accepted 2007; February 2 Received c nom Healthcare Informa g fMcoraim;Lmt fLife of Limits Microorganisms; of ogy Ecol- Astrobiology; diversity; Microbial Extremophiles; 31329 2007 33:183–209, 183 tv Hvle eedsrbdi 96(clpre al. et (Schleper 1996 in described were 1996). values pH genus ative the of species acidophilic hyper- the and found, were acidophiles lithotrophic thermophilic was described aci- rooxidans be obligately to first the bacterium but dophilic conditions, 4–6) (pH acidic slightly order: chronological following the in discovered Extremophiles were microorganisms. different of spectrum wide a by with inhabited environments are the parameters that climatic out and find physico-chemical extreme to time took It zone. dead a considered as were tempera- pressure) and body mineralization, human pH, ture, the to (compared parameters aggressive ex- time, long were a tremophiles For concerns). ecosys- environmental marine of and (because freshwater tems and importance), medical the to deep radiation). in and and (pressure ecosystems (pressure), lithospheric ecosystems classifi- underground this deep-sea to in added 1: (Pikuta be Table shown could cation factors are Additional communities 2005b). al. microbial et of 1 Table types In levels. known subspecies all or species the character- on specific differ which other istics and consistency, color, shape, size, colony,the the is cultures archaeal and bacterial for structure ganized self-protection, support, system distribution. energy effective and more allow gradi- physicochemical that to and ents and space functions their in to distributed according are all time species structures different complex of these cells In microbial mats. microbial and biofilms colonization benthic in the by of presented is form nature organized in life highest prokaryotic the organism), whole organs, sys- organs, of (tissues, tems eukaryotes of contrast structure In multicellular the populations). to and evolutionarily (consortia and communities related adjusted most rare functionally rule, a very the As is species. contain single it ecosystems a by nature inhabited is In ecotope an relations). and when species environment (cross the with itself interacting within Earth on places possible ogaoi a nw htmn ug ol rwin grow could fungi many that known was it ago Long (due body human are: ecosystems best-studied the Currently (formally er incognita terra hoailsferrooxidans Thiobacillus nvitro In fcus,tems rmtv or- primitive most the course, of , ic h niomnswith environments the since , Picrophilus cdtibclu fer- Acidithiobacillus rwn tneg- at growing .Subsequently ). priori a Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 9 cdpii eohlc040215–40 15–40 0–2 0–4 moderately Acidophilic 20. mesophilic Acidophilic 19. 3–30 8.0 moderately Halophilic 18. mesophilic Halophilic 17. psychrophilic Halophilic 16. 15–40 Haloalkaliphilic 13. moderately Alkaliphilic 11. mesophilic Alkaliphilic 10. 184 1 cdpii hrohlc70–120 thermophilic Acidophilic 21. 15–40 70–110 moderately Haloalkaliphilic 15. mesophilic Haloalkaliphilic 14. thermophilic Alkaliphilic 12. ail ulse)ta a sltdb ahfiadLoveley and Kashefi 130 at time by of periods 121(not isolated short for survives was (2003) strain that published) microorganism, validly hyperthermophilic Another ree16) n o h aiu eprtr o rwhat growth for temperature 113 maximum the now and 1969), Freeze of discovery the microorganisms by thermophilic triggered of was study the of epoch modern The ther- described already mophilic had (1866) Brewer but (1888), Miquel to qipdcl om thsbcm osbet td rl psy- truly study to well possible and become devel- instruments has the cooled it rooms of with cold technique Now equipped special with- 1909). a ago Heurck of (Van years opment term hundred this one using then out more studied been already ye fcmuiisp %(w/v) pH communities of Types cmd-ile n10 o h ecito fbcei capa- 0 bacteria at of growth description of the ble for 1902 in Schmidt-Nielsen .Mrn hrohlc70–120 15–40 0–1 9–11 70–110 psychrophilic Alkaliphilic 3–4 9. thermophilic 8 Marine 8. 15–40 moderately Marine 7. meso-thermal Marine, 6. psychrophilic Marine 5. thermophilic Freshwater 4. 0–1 5–7 moderately Freshwater 3. meso-thermal Freshwater, 2. psychrophilic Freshwater 1. h icvr ftempii atrai eeal attributed generally is bacteria thermophilic of discovery The h rtmnino h em“scrpie a aeby made was “psychrophile” term the of mention first The ◦ thermophilic thermophilic thermophilic psychrophilic thermophilic thermophilic thermophilic a on for found was C Chlamydobacteriales nw ye fmcoilcommunities microbial of types Known ◦ Mrt,17) u rtcdaoshad diatoms Arctic but 1975), (Morita, C yoou fumarii Pyrolobus AL 1 TABLE rmtegyeso California. of geysers the from hru aquaticus Thermus –03–25 9–10 (Bl¨ al Temperature, NaCl, eh ta.1997). al. et oechl ◦ Cwn2004). (Cowan C Bokand (Brock 50–60 50–60 50–60 50–60 50–60 50–60 < < < < < ◦ .V IUAE AL. ET PIKUTA V. E. C 10 10 10 10 10 eilgot i ueclue a eemndat determined was culture) pure (in bac- growth anaerobic and terial aerobic Labo- the NASA/MSFC/NSSTC Astrobiology at our ratory in Firstly microorganisms. chrophilic croorganisms hspito iweteeaiohlcognssrpeetgreat represent organisms acidophilic extreme view of point this Microorganisms Acidophilic 1. of (direction life of evolution phenotype). the and in questions changes distribution, fundamental origin, the the each to of of answers biocoenosis complex provide in will ecosystems, taxa ecosystem all extreme of in comparison the life and represent organisms prokaryotic life. of about limits discussion logical the the for issue important very this a forms is therefore, capacity and life extremophiles, first anaerobic were the Earth that early remembered on be should it extremophilic However, to life. imperative as considered reason not this is For extremophiles. anaerobiosis not an are them of most anaerobic and obligately many species, are there of archaea and bacteria cultivation the (Hungate Among later 1969). the much developed 1861), for was (Pasteur microorganisms technique anaerobic work anaerobic fermentation an his but in Pasteur by covered 2003). al. et (Edmond recently of kGy 30 resisting or- other hyperthermophilic sulfur-reducing the all archaea Among to 1960). al. lethal et are (Raj ganisms that stor- doses and at other conservation and assaults irradiation DNA-damaging food ionizing survive of could bacterium process This age. the during found al. was et (Yayanos MPa 100 at detected highest was the 1979). life and temperature, of high limit to known require addition that in microorganisms pressure are Smokers there high Black that the shown was In it crafts. studies submersible deep-ocean of ment ihsln ol n ae,adnwtercr fgo growth good of record the now and for lakes, and soils saline with and as such genera separate to microor- belonging alkaliphilic ganisms truly but 1982), Akiba and (Horikoshi soils alkaliphiles Extreme genera bacteria 1922). to belonging Lipman nitrifying and alkalitolerant (Meek about published was article an earlier years faecalis coccus 1999). Gosink and (Staley previously reported utvtdarbcbceilclue nsldaa ei loat also media agar solid − on cultures bacterial Hoover successfully aerobic colleges and cultivated Russian Pikuta our and 2002; 2003b), al. al. et Pikuta et 2003; (Hoover media solid and liquid 5 ti elkonta rtisdntr tlwp,adfrom and pH, low at denature proteins that known well is It and eukaryotic both systematics, of view of point the From dis- was life, aerobic the to alternative an as Anaerobiosis, bacterium radioresistant first The develop- the after possible became barophiles of study The td fhlpii irognsshssatdfo work from started has microorganisms halophilic of Study h rtmnindaklpiewstebacterium the was alkaliphile mentioned first The ◦ aoea mediterranei Haloferax Glcisye l 05.Teosrain flvn mi- living of observations The 2005). al. et (Gilichinsky C Natronococcus nsitu in hroocsgammatolerans Thermococcus Dwi n rikhn 98,btseveral but 1928), Cruickshank and (Downie Clostridium eedsrbdltr(idl ta.1984). al. et (Tindall later described were γ t–20 at irdainwsdsrbdcomparatively described was -irradiation ◦ a endmntae t3%NaCl. 30% at demonstrated been has nhgl ieaie ei were media mineralized highly in C and Bacillus enccu radiodurans Deinococcus Natronobacterium eeioae from isolated were hti aal of capable is that − 5 ◦ Strepto- Cona Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 piu ffnto cusa o pH. their low and at cellu- acidity occurs extra function high the of to However optimum adaptation 1998). exhibit usually Johnson between proteins and at lar (Norris measured been 7 has and acidophiles 5 pH. of low extremely pH to internal adapted be The to need from not enzymes do intracellular organisms these and cytoplasm, of inside a pH maintain to neutral ability the have microorganisms acidophilic Some u hyaeas aal ftecnupino rtnthat 4): proton (equilibrium waters a mine of some consumption in alkalinity the to of lead capable can also are they But lahn) cdpie omaii ei eulbi 1–3): (equilibria media acidic (bi- form rocks and acidophiles minerals oleaching), from iron and sulfur of transformation process of the in participating Usually single molecules. iron, a organic hydrogen, or to from sulfur, energy reduced receive to be able could are They wall membrane. micro- cell the sometimes and gram- aerobic, the stain, to reaction negative or positive spore-forming, a these have of microorganisms membranes cell The are non anaerobic. obligately They or aerophilic, hyperthermophilic, and species. mesophilic are spore-forming and there thermophilic, acidophiles moderately Among meta- bolisms. chemoorganoheterotrophic or chemolithomixotrophic, medium. surrounding the copper, in zinc of and concentrations cadmium high arsenic, with and acid cytoplasm sulfuric the between concentrated barrier Iron only in the and is drainage wall, membrane cell cell mine a the have acid not does in species 0 This California. pH ex- Mountain, at Another growing 1996). eubacterium al. is et microorganism (Schleper acidophilic tremely Japan moderately in a with spring gases within hydrothermal grow a solfataric near archaea found were these and regime of thermal cells pH minimum The a –0.2. at exist of could life that demonstrated How- and 1999). records (Pick 1 pH archaea at the ever, occurs organism this for maximum alga and geologi- are acidophilic fungi: extreme which are wa- other Hawaii, eukaryota Three and for islands. “soils” except young relatively acid world cally hot, the over colonizes all it ters and chloroplasts, C-phycocyanin its and “a” in chlorophyll contains eukaryotic It but rhodophytes. prokaryotic to not be to found microorganisms. were 0 grow- pH acidophiles near extreme of ing representative first inter- the exceptionally that is esting It 2001). Mancinelli pH and below insects (Rothschild or been 2–3 plants and not 4, have pH below molecu- cyanobacteria nature in and living the found Fish for research. genetic significance and and lar biotechnology for potential atragoiga Hls hn30hv chemolithotrophic, have 3.0 then less pH at growing Bacteria rcoprncerebriae Trichosporon uailaacidophila Dunaliella FeS S 2 2 O 2Fe + 3 2 − 2 6Fe + + Fe + yndu caldarium Cyanidium irpiu oshimae Picrophilus 2O 3 3 + + 0 2 . + + cntu yaim Cephalosporium cylatium, Aconitium 5O + 3H 3H 2 H + 2 2 2 O O O a uvv tp ,bttegrowth the but 0, pH at survive can 2H Shee ta.19) h green The 1995). al. et (Schleper ↔ ↔ ↔ + Fe(OH) 7Fe 2SO ↔ erpam acidarmanus Ferroplasma 2 2Fe 4 2 + and − IRBA XRMPIE TTELMT FLIFE OF LIMITS THE AT EXTREMOPHILES MICROBIAL sardagebelonging algae red a is + + 3 3 + S + .torridus P. 2H + 2 O 3H + H 3 2 − 2 + [4] O + 6H rk all broke + sp., [3] [2] [1] h ouiiyo easi uhgetr n nmn ae can cases many in and l g greater, the much reach is metals of solubility environments the acidic that In effects. parameters multiple such of in participate examples could are acceptance) met- wide certain received not of concentration term high (the High als and time. same pH, the low at extremes temperature, several to adaptation an velop ino oltdevrnet n o h xrcino certain of extraction the for and bioremedia- environments in polluted applied of widely tion now showed are (1982) processes al. Bioleaching of et growth Wong of metals. inhibition these containing from isolated sites were the acidophiles different of number environ- a acidic and Uranium, in ments, found 1992). were al. also chromium et and (Johnson molybdenum, respectively Fe(III), mM 300 cryptum Acidiphilium metallicus are As(III) concentra- of toxic tions the of to resistant examples archaea The and bacteria uranium. acidophilic ferric and silver, chromium, mercury, molybdenum, nickel, iron, cadmium, for studied zinc, extensively copper, resis- were arsenic, Metal acidophiles targets. of cellular mechanisms of extra- sensitivity tance barrier; or in permeability reduction intra- metal a (5) (3) by and toxic conversion; exclusion the enzymatic (4) of sequestration; (2) efflux cellular cell; (1) the metals: of to out resistance level cellular increased an convey of that 2003) al. basic et five (Dopson are mechanisms There integrity. membrane sites cellular binding disrupting native and their from anions metals with essential displacing bonds sys- tems, transport coordinate inhibiting enzymes, forming of groups by functional blocking can effect metals toxic Intracellular a toxic. transport exert become expressed they constitutively whereby unspecific, systems, of action the concentrations by physiological normal the above accumulate may h rwhsbtae n tanrssatt 5 M(0gl g (10 mM 153 to al. resistant strain et One (Dew substrate. mM growth to 800 the Zn(II) to of tolerant toxicity be The could 1999). Cu(II) of levels high rvossle xoueti pce a oeatt M(108 mM 1 to l tolerant mg was species this exposure silver previous ina ocnrto f0.93 of concentration to a toxic at is tion silver (1996) al. et to De According silver, As(III). studied: and ions uranyl, and zinc, copper, metals cobalt, the cadmium, of toxic most the is Ag(I) that 5 ar- centration the that resistance showed mercury colleagues chaeon for and available Huber is prokaryotes. data among much Not 1999). al. et of strains in mM 10 docaldarius was archaea in resistance maximum an of and number a Acidophilic include 1985). Cd(II) to al. resistant et bacteria (Trevors thiosulfate on growing 92 when to sensitive is Fe(II) on growing while Zn(II) ehv led icse htmcoraim ol de- could microorganisms that discussed already have We − 1 gI Erih1984). (Ehrlich Ag(I) ) Acidocella ealsheasedula Metallosphaera t ferrooxidans At. Crespectively. BC − μ and 1 metallophile Hbre l 99.Ga ta.(99 found (1989) al. et Guay 1989). al. et (Huber M ocnrtos nclso cdpie h metals the acidophiles of cells In concentrations. .solfataricus S. tanrssatt 0 MC(I,wiethe while Cd(II), mM 700 to resistant strain cdtibclu caldus Acidithiobacillus aebe hw ob eitn o50and 500 to resistant be to shown been have t ferrooxidans At. a sdi oeltrtr,bthas but literature, some in used was a oeaeu o1MN(I (Dew Ni(II) M 1 to up tolerate can t ferrooxidans At. μ etsiilmferrooxidans Leptospirillum ssniiet ecr tcon- at mercury to sensitive is 01 gl mg (0.10 M Dpo ta.20) Adapted 2003). al. et (Dopson t ferrooxidans At. t ferrooxidans At. by Uand KU − tan dpe to adapted strains > Acidiphilum 1 μ 5m Cr(III). mM 15 ,hwvrafter however ), uflbsaci- Sulfolobus 06m l mg (0.6 M eed upon depends eI)oxida- Fe(II) Sulfolobus spp. 185 and − − 1 1 ) ) Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 aiu ehnsso eitnet easadlw[H low and the metals environments, to resistance pH of low mechanisms inhabiting various microorganisms of sity coal. oxi- of and desulfurization the component; in feed applied processing; in are starch used dases are the cellulases in and applied proteases are glucoamylases and lases metabolism). de- of mesophilic without characteristics tailed only described were but strains (psychrotolerant 1998), conditions Johnson 1995; reported species al. were ecosystems et con- permafrost (Schleper identifi- made in of acidophiles were cases of reports The cation acidophiles. no psychrophilic and truly absent, and cerning are genera taxa of the specialized acidophiles levels psychrotolerant the among and Alternatively, on families. distant positions absolutely phylogenetic have separate sometimes species thermophilic moderately and hyperthermophilic microorganisms acidophilic John- and (Hallberg more 3 be pH 2003). to of son waters appear in bacteria particularly oxidizing significant, sulfur and of aci- iron participation moderately dophilic However, minor prokaryotes. with acidophilic occurs that extremely oxidation showed drainages iron contribution mine ferrous the acid the of for calculation processes The bioleaching method. of vi- other economically any be by not would able that ores low-grade from metals 186 udt fmmrnst ehllvl,addgaechlorophyll degrade and 75 levels, (above lethal to membranes of fluidity ssaedvddit he rus oeaeythermophilic moderately 50–60 groups: at three optimum into (growth divided are isms microorgan- thermophilic all Traditionally temperatures. higher domains other two of bers hn70 than 100 Thermophiles of Diversity Microorganisms Thermophilic 2. for taxa specialized them. non acidophilic correspondently psychrophilic obligate and of microorganisms absence of fact as the prokaryotes as of well systematics the hy- in taxa the distant separate of senting families the repre- and by acidophiles thermophilic genera supported moderately and specialized is perthermophilic Earth of early existence the of on fact environment ecosystem temperature primary high a and as acidic the original in ancient precisely the biota concerning of view distribution and of development, point origin, Our the stages Earth. earliest on resulted evolution the have biological during of possibly processes could adaptive acidity widespread from aggressive in microorganisms survive these a of have to ability not The did root. extremophiles) ancestral of that monophilic group conclude major to a us (as leads acidophiles represented, structures cell divers the Archaea osdrto ftewd pcrmo hlgntcdiver- phylogenetic of spectrum wide the of Consideration pH at growing acidophiles from Enzymes of taxonomy and systematics in that noted be should It o otkonseisof species known most For ◦ sal eauepoen n uli cd,ices the increase acids, nucleic and proteins denature usually C ◦ Acidithiobacillus ) n yetempii otmmhge hn80 than higher (optimum hyperthermophilic and C), oss ffu hl:Ceacaoa(Sulfolobales- Crenarchaeota phyla: four of consist ◦ ) aigpooytei mosbe oemem- Some impossible. photosynthesis making C), eefuda uvvn unfavorable surviving as found were Bacteria ◦ ) hrohlc(piu higher (optimum thermophilic C), Eucarya and h eprtrsaround temperatures the Archaea < –,sc samy- as such 2–3, rwa much at grow .V IUAE AL. ET PIKUTA V. E. + ,and ], ◦ C). 02.Ti ocluewsioae rmasml fama- 98 a and 70 of between sample strictly conditions under grows a anaerobic and from Iceland, near isolated system al. hydrothermal et was rine (Rachel membrane, co-culture Archaea outer the This among an 2002). exception possess notable a symbiont is this which of Cells KIN4/1. upon dependent obligately lives and sym- number, hyperthermophilic nano-sized “ a biont by represented is 2003) quotations). in (the validated written not phylum remains of establishment name its reason, organisms, this of for cultivation and from pure obtained without DNA environment of natural analysis the al. from et identified Burggraf been 1994; has al. 1997) et (Barns phylum “Nanoarchaeota.” “Korarchaeota” and The “Korarchaeota” branch), halophiles- Methanogens (extreme Euryarchaeota branch), Thermoproteales anducagd hsmasta “ of that density means cell This unchanged. the mained while 10-fold, about raised ohg ocnrtoso H of concentrations high to re ftemmeso Krrhet”ad“Nanoarchaeota” and “Korarchaeota” of members the of eries Crenarchaea all in served Furthermore, reaction. trans-splicing a of “ way by is other be halves tRNA which to of thought in joining and position intron, the an contain at tRNAs archaeal occurs tRNA pre- splitting described 4 the been and and not has viously, protein-coding genes tRNA (11 of genes splitting The split genes). of number genome. large primitive a shortest original “ of the study of is genetics elimination The it the if to or attributable is genes it unused “ if show of will size study genome tinuing the that shown was equitans It “ differed. of sequence others the two to identical East was the Rise from LPC33 Pacific for sequence The CU1). and OP9, (LPC33, biotopes temperature high environmental the from received “ were of sequence RNA of 16S the members the within even between but only domains, not different occurs that parasitism demonstrated or co-culture This symbiosis excluded. not is also KIN4/1 “ of lifestyle microorganism asitic “ “host” of the growth for with required contact was cell direct con- the that in clusion resulting failed, have membrane semipermeable a cells co-culture by the of separation active with experiments physiologically Even a culture. require they and KIN4/1, cells Separated suspension. tans” in freely of occur 80% and cells about coculture, the “ of the phase growth exponential late etaini h eim ycagn h a itr flow mixture gas the changing By (H medium. the in centration “ for min (70 times nraetespl fH of supply the increase .equitans N. .equitans N. 2 nte hlmo rhe,“ archaea, of phylum Another :CO .equitans N. ol o rwo elhmgntsof homogenates cell on grow not could aorhemequitans Nanoarchaeum 2 40k)i h mleto l known all of smallest the is kb) (490 ” = 02)t 0lmin l 30 to 80:20) )wsosre t90 at observed was ”) noe v ftenn rtista r con- are that proteins nine the of five encodes ” Euryarchaea Mkrv n onn20) usqetdiscov- Subsequent 2005). Koonin and (Makarova el eahfo h ufc of surface the from detach cells ” Igniococcus .equitans N. .equitans N. 2 h eldniyo “ of density cell the , u hyaentfudi n fthe of any in found not are they but , .equitans N. 2 .equitans N. .I sitrsigta uigthe during that interesting is It S. − htde o vnhv strain a have even not does that ” eaieto relative ” tanKN/,ad4 i for min 45 and KIN4/1, strain 1 Nanoarchaeota hwdta hsseishas species this that showed ” oalwrmvlo H of removal allow to ◦ ,p ,ad2 alcon- NaCl 2% and 6, pH C, .equitans N. ”treohrsequences other three ,” Archaea ”Frhroe h par- the Furthermore, .” ◦ .Mnmldoubling Minimal C. Igniococcus Igniococcus Igniococcus .equitans N. .equitans N. nadto to addition In . Archaea Ignicoccus Hbre al. et (Huber ” ssensitive is ” Igniococcus Igniococcus N equi- “N. 2 Con- . and S ”was strain strain strain ”but ,” re- N. Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 00 ihtmeaueotmmfrgot t50 at growth for optimum temperature with 2000) hlmCasOdrFml Genus Family Order Class Thermoprotei Crenarchaeota Phylum uyrhet ehnbcei ehnbceilsMethanobacteriaceae Methanobacteriales Methanobacteria Euryarchaeota iin.I al h urn aooyo ail pub- the validly of of hyperthermophiles taxonomy The current presented. is the po- archaea 2 phylogenetic lished Table well-established In have sitions. and validated, been the validate also could species phyla. these new of status published validly a with ∗∗∗ ∗∗ ∗ l te hl ftedmisBcei n rhe have Archaea and Bacteria domains the of phyla other All l reso hscasaeecuieyhprhrohlco hrohlc(th2003). (Itoh thermophilic or hyperthermophilic exclusively are class this of orders All hs lse osntcnantempii pce teol xeto is exception only (the species thermophilic contain not does classes These hrohlcseiso h genus the of species Thermophilic “Methanomicrobia” rhegoiAcaolblsArchaeoglobaceae Thermococcaceae Archaeoglobales Thermococcales Thermoplasmataceae Archaeoglobi Thermoplasmatales Methanococcaceae Thermococci Methanococcales Thermoplasmata Methanococci ehnpr ehnprlsMethanopyraceae Methanopyrales Halobacteria Methanopyri ∗∗ Methanococcus ∗ IRBA XRMPIE TTELMT FLIFE OF LIMITS THE AT EXTREMOPHILES MICROBIAL aooyo aiae hrohlcarchaea thermophilic validated of Taxonomy ∗∗ ◦ C). are: uflblsSulfolobaceae Sulfolobales Desulfurococcaceae “Caldispheraceae” Desulfurococcales “Caldispherales” Thermoproteaceae Thermoproteales aoatrae Halobacteriaceae Halobacteriales Methanosarcinales Methanomicrobiales .temltorpiu,M jannaschii M. thermolithotrophicus, M. AL 2 TABLE r ersne ymmeso h resThermotogales orders genera the of the members (including by represented are species. there mesophilic and orders, hyperthermophilic non- methanogenic both are the and Among methanogenic orders. both methanogenic include Euryarchaeota phylum mn h atratode-rnhdadsotlineages short and deep-branched two Bacteria the Among aoergn thermotolerans Haloterrigena Pyrodictiaceae Thermofilaceae “Ferroplasmataceae” Picrophilaceae and , Thermotoga .igneus M. PR5 T . Mnav-orge tal., et (Montalvo-Rodriguez , Thermosipho Sulfurococcus Metallosphaera Sulfolobus Stigiolobus Sulfurisphaera Acidianus Acidilobus Stetteria Thermodiscus Igniococcus Thermosphaera Sulphobococcus Aeropyrum Staphylothermus Desulfurococcus Caldisphera Vulcanisaeta Caldivirga Thermocladium Pyrobaculum Thermoproteus Pyrolobus Hyperthermus Pyrodictium Thermofilum Geoglobus Ferroglobus Archaeoglobus Paleococcus Pyrococcus Thermococcus Thermoplasma Halloterrigena Methanococcus Methanothermus Ferroplasma Picrophilus Methanopyrus and , 187 ∗∗∗ Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 sntp .Ol t25 at which Only pH, 7. neutral pH to refers not state is standard ecosys- biological underground deep the and tems, deep-sea im- for is that, it note But to anaerobic. portant and aerobic be could They alka- etc.). groups: liphiles, neutrophiles, physiological acidophiles, several ther- moderate into acidophiles, all extreme divided potential redox be and could salinity mophiles chemical pH, other stable to some Relative highly and reagents. solvents, usually organic detergents, are against besides stability, hyperthermophiles, high-temperature of having Enzymes (Sakuraba 2002). synthetase Ohshima acetyl-CoA and ADP-forming and oxidore- enzymes— ductase, pyruvate-ferredoxin novel synthase, of phosphoenolpyruvate oxidoreductase, number ferredoxin glyceraldehydes-3-phosphate a inase, includes phosphofruktok- ADP-dependent glucokinase, and ADP-dependent modified be n r eedn pnetra lcrnacpos(sulfur, acceptors metabolism. fermentative In electron have catabolism or external oxygen), respiratory nitrate, upon sulfate, have iron, dependent them are of Some and them. de- among secondary cur oc- anabolism and and heterotrophic produc- and primary mixotrophic Chemolithoautotrophs with primary as community. organotrophs well the be within as could matter, composers They organic biotopes of 1998). their ers to Stetter adjusted and well usually (Huber are they and diversity, Thermophiles of transfer Physiology genes evolution. horizontal life’s of of stages latest result the during in the diversity probably enormous phylogeny, have bacteria thermophilic Moderately Aquifex Fervidobacterium 188 ersn etaiy u ttepesr fwtrstrto and saturation water of pressure 100 the at but neutrality, represent n eeaeaegnrlytxct irognss however, microorganisms; to toxic crenarchaeon Arsenate the 2003). generally Adams are and selenate (Holden and metalloids or ions ocean). metal dis- the of widely bottom less the at are least (at springs acidic hot then tributed alkaline nature, in However, Kerlingarfj¨ the of species example for genus species, endemic are there mophiles sulfides, as sulfur, even matter, and organic hydrogen, of genus oxidation the water by of grow or Members acid product. end sulfuric an sulfur, forming as of hydrogen, or oxidation sulfide, by hydrogen autotrophically genus growing the aerobes of strict Members aci- extreme 1). among Section acidophilic (see most dophiles the as record the hold still 2005). Teske and (Amend h hsooyo hrohlcmcoraim a wide a has microorganisms thermophilic of physiology The oehprhrohlsapa ob ihyaatdt toxic to adapted highly be to appear hyperthermophiles Some alkaliphilus Thermococcus ther- neutrophilic and acidophilic moderately Among genus the of species thermophilic Moderately .furiosus P. ◦ ,tenurlp s61,ada 200 at and 6.13, is pH neutral the C, Methanothermus n hyaealhprhrohls(th2003). (Itoh hyperthermophiles all are they and ) l onan nIead(tte ta.1981). al. et (Stetter Iceland in mountains oll .brierlyi A. h mdnMyro aha a on to found was pathway Embden-Meyerhof the yoauu arsenaticum Pyrobaculum n qicls(nldn n genus one (including Aquificales and ) ylahn fsldcores. sulfidic of leaching by eefudol nhtsrnso the of springs hot in only found were ◦ n a rsuede h H7 pH the does pressure bar 1 and C sal ogo pt H10.5. pH to up grow to able is Acidianus ◦ ,i rp o5.64 to drops it C, sltdfo hot a from isolated Sulfolobus Picrophilus r beto able are .V IUAE AL. ET PIKUTA V. E. are n euigvrosmtl uha e(I) V) Tc(VII), (VI), 100 U at (III), Mn(IV) Fe and of as Co(III), such capable Cr(VI), extract metals yeast is various or it reducing peptone but and of components selenium, or or hydrogen arsenicum oxidizing acceptor. reduce electron the unable as is selenate mM arse- and mM 50 10 or hydrogen using nate sources on carbon and grows energy as Italy, dioxide carbon Naples, near spring freshwater u qai netr rgntdudrhdottcpressure hydrostatic under originated ancestors aquatic our aim Brlt 02.Hmnd vle ta atmospheric ( an MPa 0.101 at of evolved pressure Hominids 2002). (Bartlett macroor- ganisms and microorganisms both of distribution and evolution Microorganisms Barophilic 3. have may forms essential 2002). life for (Fujiwara earliest genomes required small the are had that which suggests of This most functions. genes, with packed 2003). Poulos and (Yano increased oligomerization stacking, increased aromatic asparagines, and capacity; metal-binding in cysteines, increased interactions; increase as hydrophobic an (such glutamines); residues labile and structure; in secondary in decrease increase a in concomitant decrease a a and include length These loop stability. fac- thermal several increase identified that have tors engineering) protein and structural analyses, comparative the and evolution, directed the databases, isolated were from polymerases DNA and oxidoreductases, dehydro- like genases, enzymes intracellular and pullulanases, xy- or proteases, lanases amylases, (Haney like enzymes residues Extracellular 1999). hydrophobic al. and et pro- charged thermostable many that contain shown con- was teins it denatured Also in anticipated. structure is native ditions the 2001), Zeikus retaining and that (Vieille rate indicating and unfolding slow 1997), very Regan a and show they (Nagi proteins mesophilic than contents higher show generally proteins Ther- mostable 2005). al. et (Li thermozymes called are thermophiles from cus raim o xml mlpluaaecudhv ciiyup 142 activity to have could original amylopullulanase the example than for optimum organism; temperature higher a have can zymes lcrndnrfrF(I)rdcae ciiy(K activity reductases Fe(III) for donor electron 2001). c of Lovley species and as (Childers such reducers iron cytochrome and islandicum oeaeytemsal (45–65 stability: thermostable temperature of moderately range their by defined 2003) Poulos and mM). 3.33 n xrml hrotbe( thermostable extremely and − rsuei e hsclprmtr hc a nune the influenced has which parameter, physical key a is Pressure densely be to appear hyperthermophiles of Chromosomes utilizing studies large-scale (i.e., methods principle Three hrotbeezmsaecasfidit he rus(Yano groups three into classified are enzymes Thermostable yectcrmsadisNDHi etrta AHa an as NADH than better is NADPH its and cytochromes type p. n te hyperthermophiles. other and spp., hrooamrtm,Prccu uiss Thermococ- furiosus, Pyrococcus maritima, Thermotoga ◦ Shlgre l 93.I oeltrtr h enzymes the literature some In 1993). al. et (Schuliger C cusb ehns htdfesfo h NADH- the from differs that mechanism a by occurs c dpnetpoesta cusi mesophilic in occurs that process -dependent = atmosphere 1 > .islandicum P. 85 ◦ ) hrotbe(65–85 thermostable C), ◦ Shewanella ◦ ) yetempii en- Hyperthermophilic C). .Teio euto in reduction iron The C. = α hlcland –helical .1 a) although bar), 1.013 osntcontain not does and m .islandicum P. = Geobacter .4and 0.04 β –sheet ◦ C), P. Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 rwa rsuemr hn10Maa 2 at MPa 100 isolate than This more 1979). pressure al. et a (Yayanos at 1979 in grew m 10,500 of depth a rsuesri B75ge nya 4 isolates at these only atmospheric grew of At DB6705 Most physiology. strain m. pressure psychrophilic 2500–6500 and sed- of barophilic deep-sea depth had of pres- a high samples several from from reported iment isolated have bacteria 1996) al. adapted et sure Kato 1995; (Kato al. coauthors et with thermophiles, Kato psychrophiles. alkaliphiles, and barophiles, as three such extremophiles be various to found and bacteria was non-extremophilic biodiversity fungi, The actinomycetes, weeks. of: 1–4 composed for MPa 100 at or olce rmteMraaTec.Teaa ltsi hsin- this 4–75 in at plates incubated agar The were samples Trench. vestigation mud Mariana the the from from collected microorganisms of thousands isolated e tteErhssraede o omlyocraoe100 above occur normally not does surface Earth’s the at ter 0Maa eprtrseceig100 exceeding temperatures at MPa 40 u,i ra rudhdohra et,tetmeauecan temperature the vents, 400 to hydrothermal rise around areas in but, ogo etra ihtmeaueta ttelwrtempera- lower the at than temperature high at better grow ( to pressure high of conditions At ex- ( world temperature a low is and pressure sea high deep extremely the to of posed bottom The psychrophiles. hyperthermophiles into and divides Biodiversity usually MPa atmosphere. ecosystems one 40 deep-sea of pressure then of a less at well pressure barotolerant grow can at whereas and growth MPa, optimal 40 display then bacteria more pressures at growth al. et (Kato MPa 50 below not but MPa, 1998). 80 to 70 at species grow level, piezophilic can obligately and that sea an by temperature below inhabited standard also m at is It grow 10,898 pressure. that at organisms floor harbors it sea yet deepest Trench world’s a Mariana and The the lethal. pressure, is be high could pressure very of to change adapted sudden have Many fluidity. Earth membrane on decreased organisms in resulting lipids of aging (Whitman ground 1998). under al. occurs et biosphere the number largest in the prokaryotes that of predicted is sur- It the 1994). below al. m et (Szewzyk 3500 face as deep as found were microorganisms of Siberia, communities Subsurface in Antarctica. in Baikal Vostok Lake Lake and Russia, include They the regions. and subsurface lakes deep al. deep et include (Pledger environments degrees High-pressure few a 1994). only by mi- usually but for growth, temperature crobial optimal the increase can pressure increased otmo h ca ean iuda 400 the at at liquid water remains so ocean pressure, the with of increases bottom The water level. level, sea of sea at point that above of boiling km quarter 10 a almost by is that pressure atmospheric so altitude, Pres- with pressure. lithostatic decreases for sure meter per depth, kPa meter 22.6 per kPa with 10.5 compared of rate a at increases well pressure ( drostatic as m 11000 MPa approximately 38 of of depth pressure maximal average a an as thus and average m an 3800 have of oceans depth The 2001). Mancinelli and (Rothschild aohlcbcei r enda hs ipaigoptimal displaying those as defined are bacteria Barophilic pack- compresses and volume the changes pressure Increased ◦ .Tefis aohlcbceimwsioae from isolated was bacterium barophilic first The C. > 0Ma hssri a able was strain this MPa) 50 ◦ tamshrcpressure atmospheric at C ◦ ◦ IRBA XRMPIE TTELMT FLIFE OF LIMITS THE AT EXTREMOPHILES MICROBIAL .Tkm ta.(1997) al. et Takami C. ,btntaoe10 above not but C, ◦ .Snelqi wa- liquid Since C. ◦ n oethan more and C ∼ 1 P) Hy- MPa). 110 + 2 ◦ ◦ ◦ C) C, C. lwr h pia rwhtmeauesitdfo 85 from was shifted MPa temperature 60 growth at growth optimal whereas the in MPa respectively slower; 30–45 and m at m 1484 observed of 1380 were of depth of rates growth a Maximal depth 1995). al. at et a (Gonzales Trench at Mariana hydrothermal forearc South of Izu-Bonin the samples the fluid in hot vents from isolated Gonzales were 1994; al. SM-2) et (Kobayashi archaeon Another m 1998). al. 1395 et of depth a Mid-Okinawa at the Trough in vents hydrothermal of samples fluid hot and horikoshii Pyrococcus higher at iso- barophilic The more MPa. 1986). (Yayanos became 50 temperatures Yayanos than by less no obtained pressure Mariana lates at the grow from could bacteria Trench barophilic extremely Another ture. n ciedw otedeetlvl tde ( studied levels deepest the to down active present and are microorganisms living that shows rocks continental sedimentary of research The 2000). (Pedersen oxygen and drogen hy- places producing water, of of radiolysis exception cause may the radioactivity very where with all Almost anaerobic, inclusions. are fluid environments in deep and rock material, hard in unconsolidated fractures coarser, in and sediments consolidated of composition 1995). the al. on et impact (Thorseth saltwater significant paths a flow have the may weath- in therefore microorganisms the barophilic and of basement activities the acid ering through nucleic salt-water with The of stain microorganisms. circulation of commonly presence the tunnels suggesting the stains, glass specific the of penetrate tips range the micrometer and the in holes Channels, and 1998). al. cavities, et (Fisk glass in volcanic involved this of cul- were weathering the and microorganisms amorphic microscopy that with The suggest lavas evidently surface. pillow turing pillow of the on consist glass floor volcanic ocean parts Large new years. the million 30 of every rocks basement the through min. 35 fsprde el ti motn ont htteborehole and the few very that still note are to environments important deep is super it into windows wells deep super of al. et Jeanthon 1995; al. 1995). et Beeder 1994; al. et (Beeder reservoirs subterranea Thermotoga Bacte- norvegucus, that dus sub- indicating ( of reservoirs, Archaea and oil samples ria continental from and performed floor been sea isolations have Successful 1996; 1999). thermophiles al. al. et of et Crozier (Pederson 1997; al. Scandinavia et and Chandler Africa under- in investigated continental other sites as ground subsurface well as deep shown been American have sediments North in Bacteria and Archaea of communities diverse culturally and phylogenetically horikoshii n t100 at and 0Mat 90–95 to MPa 30 yetempii barophiles Hyperthermophilic h nrtretilmcoraim wl nteprsof pores the in dwell microorganisms intraterrestrial The passes water oceanic all that indicate calculations Some ocrigtecliaino irognssfo samples from microorganisms of cultivation the Concerning ◦ a bevda 95 at observed was tapesr f3 P,wt obigtm of time doubling a with MPa, 30 of pressure a at C ◦ rhegou ugds Thermodesulforhab- fulgidus, Archaeoglobus t4 P.Temxmmgot aeof rate growth maximum The MPa. 45 at C eeioae rmbceilmtsamples mat bacterial from isolated were ◦ .peptonophilus T. ne rsueo .–5MPa, 0.1–15 of pressure under C hroocsprofundus Thermococcus nai ephtoil hot deep inhabit ) ∼ srisO1and OG1 (strains .peptonophilus T. 00m.Large m). 3000 ◦ Cat 189 and P. Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 clclshv endsusdi rvosrve (Bartlett review previous a in biolog- discussed Other of 2002). been structure 1999). have the on cells al. pressure ical et high of (Marteinsson effects interesting pressure piezophilic atmospheric deep-sea der the in induced be hyperthermophile de- to upon found heat-shock piezophiles was to similarity heat- proteins, in showing The induced protein stress protein. be A basic compression. also highly may proteins small unknown shock an expo- is following pressure-inducible protein major induced The regimes. are thermal opposing stres- which to sure only proteins, the of cold-shock sets is and heat- proteins, Pressure many induce ago. simultaneously to time deep- known sor long the from a emerged environment atmospheric life sea at that growing indicating organisms environ- possibly in high-pressure pressure, conserved the be in sug- may developed results ment systems These the 1996). Bartlett that pressure and gest Welch atmospheric 1995; at al. growing microor- et bacteria (Sato deep-sea-adapted in in also only but ganisms, not found was expression 1997). al. et reme- (Wang environmental diation for and candidate recovery prime heavy-metal a in it applications making wall, cell tolerates the onto only precipitation not It mM). ( 5 completely but to (up cadmium of of concentrations strain vent mesophilic new aeruginosa Pseudomonas Another 1997). al. clotting et blood of (Raguenes onset the delays which chemical heparin, to its resemblance for interest medical potential of exopolysaccharide abolicus Mesophilic biotechnology. and medicine in plications above ther- at either 2001). growth Horikoshi are and optimal which (Abe have atmosphere of one and most psychrophilic organisms, or of mophilic from isolated variety been have wide and a pressures high at stable are zymes, 1999). al. et Kalyuzhnaya Pedersen 1998; and Motamedi 1998; al. et Kotelnikova 1998; Pedersen and (Kotelnikova bacteria sulfate-reducing and methanogens, methanotrophs, mi- of cultures subterranean pure of of isolation to study led diversity crobial The 1990). Ekendahl m and 1000 exceeding (Pedersen depths at microbial aquifers rock unknown igneous in previously ecosystems subter- revealed on program microbiology research ranean Swedish disposal the waste in studies nuclear The long-term surface. Earth’s mate- the molten beneath partly or or at rial molten of cooling through formed earth, that controls negative such 2000). good (Pedersen had from contamination them precluded microorganisms of none of reports but isolation are ecosystems, successful There Russia. the Peninsula, about Pechenga- Kola the in of occurs area deep, Zapolyarny m 12262 purpose. SG-3, microbiological well a deepest with The drilled been have them of none 190 twsrpre htahg-rsuergltdsse o gene for system high-pressure-regulated a that reported was It ap- important have ecosystems deep-sea from findings New en- piezostable as to referred currently enzymes, Barophilic the of constituents solid predominant the are rocks Igneous sltdfo etsml,scee ninnovative an secretes sample, vent a from isolated > 9)rmvstecdimfo ouinby solution from cadmium the removes 99%) hroocsbarophilus Thermococcus srmral o t oeac ohigh to tolerance its for remarkable is tcliainun- cultivation at irodi- Vibrio .V IUAE AL. ET PIKUTA V. E. n18 ose a h rtt eotmcoraim growing microorganisms 0 report to at first well the was Forster 1887 In Microorganisms Psychrophilic 4. l fgoiga 0 capa- at bacteria growing describing of in ble was 1902 loving) in (cold Schmidt-Nielsen “psychrophile” by term made the of mention first The rsrigmcoilclue ne auma eylwtem- low very –196 at to (–70 vacuum peratures under of way cultures traditional microbial a labo- is preserving microbiological freezing) (dry In lyophilization crystals. the ice ratories, of formation pre- and the from effects venting it dehydration of protect severity and the reducing cell by the freezing penetrate they and liquids, miscible 1985). (Franks crystallization dehy- ice and accompanying concentration, dration solute damage, re- membrane and to hardening, sistance frost during modifications metabolic involving tolerance, drastic freeze organ- of some mechanisms developed cry- However, have avoidance. such isms freeze of protection to synthesis the leads The as oprotectants 1995). serves (Raymond glycerol some freezing of example against production for the as 2000). fish, creatures, polar (Raymond living Sea- glycoproteins evolved Antarctic be higher macromolecular Among to all) large appear not these that (if synthesize to substances most able that are known diatoms now Ice al. is et (Raymond It activity avail- metabolic 1994). for water necessary liquid is the which making able, ice ice of surrounding pitting the the melting to and lead extra-cellular that substances produce ice-active psychrophiles and enzymes other and microorganisms. psychrophilic diatoms other avail-Some for the water increase liquid and the snowmelt of a alter ability induce organisms to snow These the of of spores. albedo species red brilliant a produce as which growth such the algae, of because snow red, of or pink colored sometimes are fields trophy. not but due cold, inappropriate of tolerance an the is to exact which cold,” the “eating since “psychrotrophic,” means term translation opti- the Here an ignore microorganisms. have specially mesophilic usually we for range they the and in temperature they growth room mum psychrophiles at unlike die but not at do phase temperatures, lag low prolonged a and with subzero growth of capable be and metabolic activity high have maintenance can microorganisms without Psychrotolerant rapidly proteins ice. in destabilize and and enzymes sensitive their very and are temperature, room at lysis cell ogo ihteasneo eaoi ciiya temperature a at inability activity 15 the metabolic than and of higher absence temperatures, the subzero with and grow low to at grow to abil- ity the is microorganisms psychrophilic bi- for current definition The ological fish. and yeasts, insects, including mosses, organisms; lichens, algae, eukaryotic diatoms, of species of number a aal fsriigde reig n hsfauepoal is probably feature life. this for and universal freezing, deep surviving indeed of are capable cells biological conditions specific under that strating okrosre iigageascae ihiei 1840. in ice with associated algae living observed Hooker rortcat uha lcrlo MOaewater- are DMSO or glycerol as such Cryoprotectants snow large of surfaces the regions, geographical Northern In ◦ htwr sltdfo s Hyu ta.2004). al. et (Hoyoux fish from isolated were that C ◦ .Tu scrpii irognssundergo microorganisms psychrophilic True C. ◦ .Ltrtetr a loue orfrto refer to used also was term the Later C. ◦ )adfrln eid ftm,demon- time, of periods long for and C) hayooa nivalis Chlamydomonas , Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 i ein(mlhnoe l 93 rtek n Khmelenina and Trotsenko 1993; Arc- al. the et of (Omelchenko methane-oxidizing water region swamp Also tic cold the Canada). in found of were (swamps and bacteria aerobic climates Russia most) psy- cold in not for in Siberia (if of search occurred many habitats the since methanogenic to methanogens, of paid of been strains has chrophilic attention more last acetogens, the decade In methanogens, nitrate-reducers. physiolog- and a bacteria, iron-reducers, following sulfate-reducers, have fermentative the that groups: in al- occur anaerobes ical other nature re- Active psychrophilic commonly environments. and also truly cold Diatoms were in yeast archaea. ported and fungi some groups cyanobacteria, and physiological gae, main eubacteria, They all broad. almost of very is eukarya, ecosystems many cold include de- from were isolated that and tected microorganisms psychrotolerant and chrophilic (troglo- light of absence psychrophiles). the in environment poor microorganisms a cracks, in evolve and also caves availability alpine In nutrient 1982). and (Friedmann water low survive het- bacteria, and cyanobacteria erotrophic yeasts, dry lichens, Antarctic the comprise of which rocks deserts, in found mi- are endolithic that The communities 2000). crobial strong al. to et exposed (Carpenter are radiation psychrophiles surface ultraviolet caps, snow polar the and On glaciers 1999). of Gosink and (Staley psychrophiles eea oa nbievisa –20 at veins brine of in concentrations salt molar to several exposed are bacteria, protozoa, comprise and which fungi, ice, algae, sea in found are that microbial communities The baro-psychrophiles). (or must piezo-psychrophiles therefore and be sediments pressures, in high extremely and with depths faced ocean are they the In 2003). constraints Gerday environmental to and further only (Feller to not also adapted but are they temperatures, as low extremophiles true are m) 1,000 e wt osattmeaueo 4 of temperature constant a ecosys- (with the global-scale of this tem surface inhabit the that of psychrophiles quarters The three planet. cover oceans since floor sea sediments permafrost the of thawing. region) undergoes summer, (active polar zone the surface of thin period a short relatively a During Yakutia). is it hundreds e.g., several meters, reach of can permafrost the On of landforms. thickness the and Earth conditions and terrain the factors extreme climatic by of by characterized controlled 20% all above The than is 2001). area, more al. land world’s underlies et (Wagner which succession permafrost, in terrestrial years more or two for odtosi hc ol n eiet eana rblw0 below or at remain sediments and soils thermal which with in ground permafrost conditions frozen of as defined of areas is enormous sediments Permafrost regions, formed. marine are polar and the water In oceans. deep of the the glaciers ice and and polar snow-caps mountains, with the high Antarctic permafrost, and and Arctic glaciers the sheets, of regions the include Psychrophiles of Diversity Microbial and Ecosystems h hsooia n hlgntcdvriyo psy- of diversity phylogenetic and physiological The h ags o-eprtr csse nErhi h deep the is Earth on ecosystem low-temperature largest The h csseso at ihpraetylwtemperatures low permanently with Earth of ecosystems The ∼ 0 o80mtiki atSbra(Central Siberia East in thick m 800 to 600 ◦ ,adaeteeoehalo- therefore are and C, IRBA XRMPIE TTELMT FLIFE OF LIMITS THE AT EXTREMOPHILES MICROBIAL ◦ eo et of depth a below C ◦ C rmngtv uft-euescpbeo rwha –1.8 psychrophilic at truly growth However, of 1969). capable sulfate-reducers al. Gram-negative et (Iizuka 1968 in lated from Antarctica bacterium sulfate-reducing Gram-positive first The 2002). nrae h udt ftemmrn eas nauae fatty unsaturated because membrane the of fluidity This the reduced. is increases temperature the when occur to found commonly the depress water. cellular further of can of point synthesis freezing peptides the and Also, length. glycoproteins chain antifreeze acid fatty the in shortening fatty of degree to unsaturation modifications the acids, of changing the of fluidity by the membranes increasing changes), flexible conformation (more con- and proteins structural of be capacities could of changing temperatures the with cold nected to the reviews, adaptation recent of to directed mechanisms According generally growth. elab- than are many rather survival strategies of at These induction responses. the cause stress can orate value ex- optimal these the require) from to away conditions environmental sometimes in Changes (and environments. treme prefer adapted to have lifestyles Psychrophiles their adapt environment. and deteriorating sense to the opportunity the to sufficient if a limits with maximum provided to is pushed cell microor- be most can For tolerance stress. this the ganisms, resist to attempting provisions or suitable survival making for and conditions stress both the by to this yielding perform could Microorganisms min- days. of or scale hours, time utes, en- the over an adapt in al. can changes and et small parameter tolerate Russel vironmental to 1986; able are (Ray bacteria yield Most biomass 1995). phase reduced lag increased and an growth has of or growth, the ceases whether killed, determines is usually organism change intensity the The of organism. duration an time on and stress conditions a inflicts environmental optimum in the from change pH, extreme temperature, Any physi- of etc. its optima salinity, in and reflected range is characteristics: as ological environments ecological natural in Temperatures Low to Adaptation of Mechanisms the inhabit that species floor. psychrophilic deep-sea truly decomposition organotrophic the for by biomass primary a provide could they but psychrophilic, not are bacteria These organic anabolism). for (require compounds photoheterotrophic are and off and on synthesis photo- switch could bacteria These 2001);bacteria vents. high-temperature al. from wavelengths et infrared Kolber using by 1996; photosynthesis perform al. could that hydrother- et black-smoker Dover near (Van floor vents sea mal deep the processes on found photosynthetic were Unique bacteria. also photosyn- but algae), chemolithotrophic only brown and not green diatoms, (cyanobacteria, includes thetic ecosystems environmental cold Sval- 1999). of al. coast et the (Knoblauch off bard sediments marine cold permanently from ihnotm fgot t7–10 at growth of optima within nauaino at cdcan stecag hti most is that change the is chains acid fatty of Unsaturation functioning optimum for adapted is microorganism Every in compounds organic of synthetics) (or producers The euftmclmantarcticum Desulfotomaculum ante-iso-/iso- ◦ eeioae nyi 1999 in only isolated were C rnhn atrs n by and patterns, branching tanN.4wsiso- was No.64 strain ◦ and C 191 Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 ii,a hc ahdsiiaoypoesocr,i correlated is occurs, process dissimilatory each which at salinity limit, maximal The dramatically. decreases types metabolic aero- diversity of the salinity phototrophs, increasing With 2002). and anoxygenic (Oren sulfate-reducers, methanogens denitrifiers, and fermenters, oxygenic heterotrophs, halophiles bic Archaea, of wide: domains: diversity very metabolic taxonomic is The three Eukarya. the and of Bacteria, each Halophiles in salinity. 15% found to up are tolerate to able but media in salts growth the upon dependent not are microorganisms Halotolerant Microorganisms Halophilic 5. homologues. mesophilic their be of could that and than temperatures higher en- low times at 10 psychrophilic active The highly be temperatures. could low zymes at rates metabolic life of to emergence compatible modification the allowing the kinetics, is enzyme psychrophiles of of strategy adaptive key 2000). The al. et (Detrich polymerization microtubule and dormancy seasonal permeability, channel ion of regulation the involve isms understood. well acclima- not of still an is function of proteins cellular tion formation The the mRNA structure. preventing in secondary chaperone and mRNA a translation, as of initiation acting tran- of the folding, level as the well at as in synthesis, are scription protein Csp cellular as of of well function regulation main as the The translation, stabilities. and protein transcription and of mRNA levels the at trolled inducible as such membrane the of desaturases. fluidity the linked maintaining also to are Others stabilize production. can protein re-initiate proteins psy- and shock mRNA differentiate Cold and mesophiles. during from temperatures, synthesized chrophiles low continuously at are growth that prolonged and com- Csps are ac- that to cold described parable the been also proteins, has pro- cold-induced (Caps) are proteins of Csps climation more group the second shock, A the of duced. severity the temperature, response. low larger at the shock synthesized and cold are proteins (Csps) during proteins of expression shock groups Cold gene two the are at There produced and drop. rate temperature the cold as different of well as 50 extent species, to the on up shock depending of proteins, Cold shock expression proteins. the involve cold-shock in- can of response the synthesis involves the It and response. duction expression—cold-shock gene in acids. an fatty thus and chain acids straight fatty mono-unsaturated cyclic in of and/or may increase proportion amount there the Sometimes, in the occur. reduction a in may be acids increase fatty an branched membrane. temperature, of cell kind in the fall of fluidity a the the After increasing would Also, of which quickly. effect shortened, the be react have may to length the chain able in acid are fatty situated average thus desaturases and by achieved itself is membrane it sat- and than membrane chains the urated to disturbances more create groups acid 192 aohlcmcoraim eur ati ei o growth. for media in salt require microorganisms Halophilic organ- psychrophilic by developed strategies adaptive Other con- and multifactorial, is synthesis Csp of regulation The alterations specific initiates temperature in decreases Sudden .V IUAE AL. ET PIKUTA V. E. in.I h rtsrtg,clsmiti ihitaellrsalt intracellular high maintain concentra- cells salt strategy, high first of the the presence In with the tions. to cope inherent to stress microorganisms osmotic enable that world microbial Environment Hypersaline the to Adaptation Kim and pur- (Joo 2005). for light photophosphorylation of tem- membrane-mediated the availability high the ple which at increases (especially in also low This brines is peratures). concentrated oxygen to molecular float in of to live pri- solubility cells are and the halobacteria aerobic since enable layers marily to surface space. is oxygenated vesicles more filled the gas gas of hol- a function are surrounding The that structures vesicles proteinaceous bac- gas aquatic low buoyant many produce Like and halobacteria light). ultraviolet light teria, and green blue towards from (swimming away response mediate phototactic that rhodopsins light- the sensory directed two and inwardly pump, an chloride driven is halobacteria, which in halorhodopsin, synthesized including also are bacteriorhodopsin, to addi- in tion proteins, retinal Several oxygen. molecular of requires cleavage that oxidative by produced is Retinal C-50 as in- such biosynthetic are termediates of carotenoids amounts smaller abundant ul- although from most bacterioruberins, resulting The dimmers radiation. thymine traviolet pho- repair active to an stimulating system for torepair necessary be which to carotenoids, shown red-orange been halobac- of have Also, quantities intensity. large light contain high teria and tension induced support oxygen is and low Bacteriorhodopsin by synthesis growth. ATP phototrophic drive of to period used a light- be a can as generated poten- membrane tial acts The it pump. proton and transmembrane and dependent (retinal), (bacterioopsin) chromophore moiety bound protein covalent a Bac- contains bacteriorhodopsin. chromoprotein, teriorhodopsin a of lattice two-dimensional crystalline a contain that special- membrane cell membrane, the of purple regions the ized A is glycoprotein. halobacteria of of like composed feature S-layer unique and wall lipids cell a ether-linked bacteria, transcrip- mechanisms, some eukaryotic-like translation including and archaea, tion the bacteriorhodopsin- of the acteristic hue form char- purple features that exhibit Halobacteria A membrane. halobacteria purple containing colonies. in pink seen or be gas C-50 may white, with of those opaque, presence and the form colorless, to vesicles are due strains vesicle some cell but col- in carotenoids, are orange particular halobacteria or in Most red characteristics, lipids. ored archaeal ether-linked of their presence of the basis the bacte- the halophilic of on from integrity ria differentiated structural be the can maintain M Halobacteria and cells. 1.5 grow require to halobacteria both Most NaCl order. Halobacteriales the in he,mmeso the of members chaea, os- of cost energetic environment. and in generated adaptation energy motic of amount the with hr r w udmnal ifrn taeiswti the within strategies different fundamentally two are There aoatraicuerdpgetdeteeyhlpii ar- halophilic extremely red-pigmented include Halobacteria β crtn n yoeeaeas present. also are lycopene and -carotene Halobacteriaceae aiy h nyfamily only the family, β crtn,astep a -carotene, Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 fmdu.Tene o Na for need concentrations NaCl The higher medium. in of cells of cultivation the at creased alga halotolerant of membrane halophilus oxidizer sulfur autotrophic 15%. halophilic above one salinities Only at found been not have oxidizers nitrite and ammonia autotrophic oxidation, complete with sulfate-reducers Au- salinities. dissimilatory methanogens, high aceticlastic at methanogens, thrive totrophic to shown been never microor- have of ganisms groups physiological other saturation, NaCl to or at close occur can denitrification and fermentation, respiration, aer- obic photosynthesis, anoxygenic and envi- oxygenic mineralized While highly ronments. the in function types metabolic known energetically are which produce. to molecules, easier smaller for with salinities highest solutions ac- the the at are preference solutes clear a organic is When there cumulated, 1999). ex- (Oren are which produce solutes, to only. osmotic pensive prokaryotes organic of use groups organisms specialized other few All be a by This can used process. evolutionary is these complex option and and long a machinery, in only intracellular achieved the of adaptations salt of concentrations intracellular molar The tre- KCl. by by 1996). represented balance al. usually osmotic is et composition the (Welsh provide glycine could and it halose time same the at is observations halophilus these to me- intracellular exception surrounding single the the The of that dia. those report to similar studies are most concentrations ionic and representatives groups, in found these been of have solutes osmotic organic Haloanaerobiales No order the Halobacteriales of bacteria order halophilic the anaerobic and of archaea halophilic extremely aer- obic groups: unrelated phylogenetically “salt-in” two The in that only. applied is compounds strategy beyond osmolytic the strategy of synthesis “compatible-solutes” the of the of cost energy lyakyrl nkeigteitaellrNa intracellular the keeping in role key a play costicola as rio such bacteria halophilic moderately from acterized o.Teatvt fteNa the of activity The low. hog hi ebae.Na membranes. salts con- inorganic their of ionic through diffusion intracellular the keep counteract to to and low pumps have centrations ion also in solutes energy osmotic expend organic to medium of the concentrations of high pressure Mi- with osmotic 1999). the (Oren balance required that is croorganisms systems adap- intracellular special the no here of and tation solutes, bal- is compatible medium organic the by of anced pressure osmotic the case salt this In low “compatible-solute” strategy). maintain (the cytoplasm cells con- their the salt within strategy, high concentrations second of presence the the In to centrations. adapted be should intracellu- systems all external case lar this the in strategy), to “salt-in” equivalent (the concentrations least at osmotically concentrations, uvyo h aohlcmcoraim hw htntall not that shows microorganisms halophilic the of survey A extensive requires option salt-in cheaper energetically The (formally htcudacmlt atisd fctpamand cytoplasm of inside salt accumulate could that htmil s rai oue.Teeantiporters These solutes. organic use mainly that hoailshalophilus Thiobacillus + /H + + + /H upn hsmyices the increase may thus pumping uailasalina Dunaliella niotr ntecytoplasmic the in antiporters + niotr aebe char- been have antiporters IRBA XRMPIE TTELMT FLIFE OF LIMITS THE AT EXTREMOPHILES MICROBIAL a enisolated been has ) Halothiobacillus + concentrations Desulfovibrio aebe in- been have Salinivib- . in rnlto,Na translation, transcrip- tion, of inhibition bacteria. includes of halocins spectrum of broad action Bacteriocidal a inhibit they halocins; called ocins (2005). Roberts by compre- reviewed hensively were strategy), “compatible-solute” saline (the highly environment a in physiology active their maintain croorganisms binding these saturate to necessary are sites. salt Therefore, of protein. folded amounts the to molar ions salt of binding specific affinity a low by explained be concen- simply can KCl stabilization the or for trations NaCl high for requirement the X-ray crystallography, by determined been has structure dimensional three whose from of case (hMDH) the In dehydrogenase salt. malate by enhanced salt effect hydrophobic high destabiliza- the offsets at from tion repulsion proteins electrostatic of The solubility concentrations. the carboxyl maintain hydrated which with halophilic groups, charged All negatively charge. highly surface con- salt are high high this proteins of shield role to the is that believed centrations to is compensated it be and somehow unfolding should avoid charge caused the surface instability high by The the achieved by charges. be close between may forces flexibility and repulsion their charge properly surface folded negative highly once a soluble all have Since enzymes concentrations. halophilic salt high at form into native fold proper to elements structural specific have concentration. cytoplasmic proteins KCl Halophilic high a in soluble and be stable to both them allow that mechanisms specific evolved Halophilic have proteins interactions. hydrophobic enhanced by destabilized remain halophiles of groups undiscovered. physiological explain “missing” may the That recommended. why isola- be for may halophiles media new enrichment of of the tion inclusion in osmolytes The of environment. kinds the different in excrete molecules and produce osmolytic may the which mi- complex of of some in types coexist, croorganisms occur metabolic high different could at where situation life communities of microbial a cost Such energy concentrations. the reducing salt when thereby environment the available, from is solutes such it up take to able also concentrations are salt high at vitro grow in to cultures pure microbial ing have processes microbial shown different been the which at concentration, (optimum NaCl 24% NaCl). to % up 5–6 at with is media in tetrationate, sulfur thiosulfate, elemental oxidizes and organism this culture; pure in h 4nwhlpii rhe eefudt eal ogo in grow to able be to found were archaea halophilic new 44 The of capable species many cellular membranes. of disruption and bacteriolysis, formation, pore activity, oeo h xrml aohlcacaapouebacteri- produce archaea halophilic extremely the of Some mi- halotolerant and halophiles allow that osmolytes The general in are concentrations salt high at proteins Usual salt upper the between exists correlation good a cases most In eetyi a hw htwti aoatraeeteeare there Halobacteriaceae within that shown was it Recently otmcoraim htpoueogncosmolytes organic produce that microorganisms Most . nsitu in oocradteaiiyo h correspond- the of ability the and occur to + /H + p nioe,DAadRAnuclease RNA and DNA antiporer, hdoyezi cddegradation. acid -hydroxybenzoic aoruamarismortui Haloarcula 193 Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 iecnann 9 l g a 290 from Sa- containing isolated Algerian were site in microorganisms of lake, halophilic study salt extreme the Golea hara, During El 2006). in al. biodiversity et soda prokaryotic (Pan Xilin Mongolia and Inner in Shangmatala, lake) (Erliannor, types lakes different three hypersaline from of isolated were archaea halophilic five sixty- and hundred One strains continues. new ecosystems hyper-saline of from isolation with work intensive the halophiles, from 2006). al. et (Cuadros-Orellana source . mM 0.4 194 o h emnaino ike n sauerkraut. drica and pickles of fermentation the for compounds. halo- by organic pollutants genated of bioremediation the for Some used are ecosystems. halophiles saline Halophiles oil-polluted derivatives. survival of acid bioremediation higher in fatty a used on stabil- thus based liposomes chemical and than esterases high rate against a resistance have and Ether-linked halophiles ity water. archaeal and from soil lipids oil-contaminated the of enhance remediation exopolysaccharides halophilic biomolecules. and of used processes Biosurfactants freeze-drying is in Trehalose cryoprotectant ex- a reaction. as for chain Ectoine polymerase cells. stabilize whole of ample, and stabilizers as membranes, used DNA, now enzymes, solutes Compatible concentra- 1M. NaCl below at denatured tions most and and inactivated enzymes proteins, these known of most denatured which or salt, precipitated of have concentrations high under proteases) functioning and of capable gelatinizes, amylases, lipases, (DNAses, zymes en- stable produce microorganisms Halophilic increasing. ously 2005). al. et (Walsh approach cultivation-independent Canada, with Columbia, investigated British was in Spring Salt at gradient salinity soil de- were phylotypes (Paˇ bacteriorhodopsin tected 16Sr- different different 15 10 result a and as RNA and in screened, were resulted that markers clones 180 molecular as Adri- bacteriorhodopsin of and rRNA crystallizers the Seˇ in atic archaea halophilic of vestigation otaklpii irognssaecaoatrata r ca- are that cyanobacteria are microorganisms in alkaliphilic at The pH most nutrition. grow optima particularly two cannot conditions, have growth and that upon species 8.0, dependence some than are higher There pH. pH neutral with media growth a Microorganisms Alkaliphilic 6. under- deep in caves. buried salt waste, ground nuclear and toxic store con- halophiles that of biodeterioration tainers Also possible of (2000). question al. the to et important as are McGenity crystals by salt reviewed ancient been more even has or found Jurassic, were Permian, halophiles some in that alive reported been has it as concern u oteboehooia motneo e molecules new of importance biotechnological the to Due h itcnlgclapiaino aohlsi continu- is halophiles of application biotechnological The laihlcmcoraim r irognssta require that microorganisms are microorganisms Alkaliphilic great of is paleontology for halophiles of significance The sue naeirto fsi aiiydrn rpgrowth. crop during salinity soil of amelioration in used is oleslen yuiggn rget noig16S encoding fragments gene using by salterns covlje p si´ hdoyezi cda h oecro n energy and carbon sole the as acid -hydroxybenzoic ta.20) rheldvriyaogatransient a along diversity Archaeal 2005). al. et c − 1 al(Hacˇ NaCl atbclu plantarum Lactobacillus n ta.20) h in- The 2004). al. et ene nbeacylin- Anabaena .V IUAE AL. ET PIKUTA V. E. sused is i.Sm fteaklpie n aolaihlsaeobligately CO are upon haloalkaliphiles dependent and me- growth alkaliphiles the the in of NaCl Some of dia. presence the require also they high and pH require microorganisms: Haloalkaliphiles at of haloalkaliphiles. are grow and groups alkaliphiles alkaliphiles physiological to main all able two (1999) are on Horikoshi but divided to pH, have According neutral organisms 10–11. at pH Alkalitolerant growth 12–13. for pH pH optimal at growth of pable itn e eeaadfmle Zvri ta.19;Zavarzin 1999; 2000). al. Zhilina et (Zavarzin and families and genera carbonate/di-carbonate new phylogenetically was distant numerous of it discovery the alkaliphiles to mineralized led for composition) highly case of (in application media was the it halophiles, as Just extreme anaerobes. for alkaliphilic of isolation were the etc.) for thiosulfate, applied (sulfide, reducers additional techniques, n ik16) fe h plcto fseicmdawith media specific of application the After 1963). Rizk (Abd-el-Malek and environments hypersaline in sulfidogenes function- of the about ing al- Abd-el-Malek confirmed of of hypothesis had discovery existing The finally long-time 2003). bacteria growth al. for sulfate-reducing et NaCl Hoover kaliphilic require 1996; them al. of et some (Zhilina found and were halotolerant, be also to spirochetes sugarlytic anaerobic Alkaliphilic tolerant tha was more bacterium of This salinity Egypt. to in Natrun Wadi lake alized het- genus (belonging the aerobic to eubacterium The alkaliphilic lakes. spore-forming soda erotrophic from isolated archaea anaerobic malcaliphilum genera Natronococcus to extremely belonging archaea alkaliphilic, halophilic aerobic, described co-researchers Oscillatoria, with Chamaesiphon, Ec- tothiorhodospira, Rhodobacter, Thiocystis, Thiospirillum, Amoebobacter, Thiocapsa, Chromatium, Lamprocystis, Calothrix, Anabaena, Synechocystis, Scytonema, Synechococcus, Nodularia, capsa, era: gen- following including cyanobacteria are microorganisms nant ( alkaliphiles extreme Bacillus of presence the Horikoshi of showed works The 1922). Lipman ear- and bacteria (Meek reported much nitrifying were alkalitolerant but about 1928), communications Cruickshank the and lier (Downie 1928 in lated laihlcmcoraim eebsdo h plctosof applications truly the of on NaCO of isolation based for composition were media chemical microorganisms the alkaliphilic the lakes of so- soda NaOH study mineralized by highly the adjusted after pH Later, high with lution. media pri- on were alkaliphiles isolated aerobic marily Historically 2000b). 2000a, al. et kaliphilum anaer- Two feces. and soils acidic obes even or neutral from isolated lakes. soda from h rtaklpii strain alkaliphilic first The ti neetn htaklpii irognsscudbe could microorganisms alkaliphilic that interesting is It prln,Croocdoss otc ynsia Gloeo- Cyanospira, Nostoc, Chroococcidiopsis, Spirulina, nxbclu pushchinoensis Anoxybacillus 3 /NaHCO nsiswt eta H nsd ae h domi- the lakes soda In pH. neutral with soils in ) eeioae rmmnr ihnurlp (Pikuta pH neutral with manure from isolated were Bacillus and Tnale l 1984) al. et (Tindall 3 ufr.Wt h eeomn fanaerobic of development the With buffers. 3 2 ehnslu zhilinae Methanosalsus − a sltdi 93fo ihyminer- highly from 1983 in isolated was ) al(ese n Tr¨ and (Weisser NaCl M 4 n os seilymcoraim isolated microorganisms especially ions, tetccu faecalis Streptococcus and ehnbceimther- Methanobacterium . Natronobacterium euftmclmal- Desulfotomaculum r xmlsof examples are Clostridium t.Tindall etc. pr1985). uper a iso- was and and Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 aiainacrigt ue6.Rfrne it editor, Lists n Reference: 61. Rule to according validation fNa of in well quite used powders). wash is and growth capacity (detergents pH this biotechnology physiological and than organisms, higher of much optimum pH at activity mal ye feteohls hr r okonmcoraim that other microorganisms known to no contrast are there in extremophiles, of However, types radiation. X-ray of by discovery sterilization remarkable the radiodurans after Deinococcus initiated was radiation high Radiation to Resistant Microorganisms 7. approaches. biochem- and ical genetic combining by achieved generally is of which depends identification the significantly antiporters, growth, cation/proton monovalent and is upon survival that homeostasis both pH for alkaline active al. important that et shown (Padan was bacilli It alkaliphilic 2005). and bacteria neutrophilic in sis diversity. total derive to of impossible out is hyperthermophiles, it like which evolution, of is line community dead-end alkaliphilic a the not that show and phylogenetic prokaryotes universal rep- of the tree of include branches to major sufficient all is of resentatives community if out this find of should biodiversity one the prokaryotes, of diversity biological rise gave the that to alkaliphilic source the terrestrial the whether reflect of indeed Protero- question can early community the the answer in to biota order continental In the zoic. of analogue relic regarded a be as can community alkaliphilic prokaryotic this the For ones. reason, of thalassic than formation rather the bodies water from inland resulted athalassic mineralization soda that fact the of consists communities between microbial difference halophilic and basic alkaliphilic the Ac- the 1999). Zavarzin, al. academician et (Zavarzin to level cording system the evolu- at occurred during had conditions tion environmental their extreme that suggest to organisms adaptation alkaliphilic of properties their transport. these ion maintain All for pathways must different realize alkaliphiles and the pH intracellular pH to Due environmental stress. high osmotic a the resist to compounds osmoprotective 2005). family separate the rep- resented and lineages posi- phylogenetic al. known found et from was distantly Zhilina very sulfate-reducers 2003c; tioned alkaliphilic al. the et of Pikuta One 1998; al. 2005). et Pikuta (Zhilina 1997; continents al. American et and Asian, African, of lakes soda thiodismutans, D. custre, sulfate-reducers of ( presence the buffers carbonate/bicarbonate eufntooirohdoeooas eufntou la- Desulfonatronum hydrogenovorans, Desulfonatronovibrio ◦ 0 (footnote). 107 laihlcmcoraim eeo thg concentrations high at develop microorganisms Alkaliphilic opti- have alkaliphiles some from enzymes alkaliphilic The h einn fasuyo irognssrssatto resistant microorganisms of study a of beginning The homeosta- pH of mechanisms the compared review recent A 1 h rgnlspelling, original The + 1 osad iial ohlpie,hv oaccumulate to have halophiles, to similarly and, ions n.J yt vl Microbiol., Evol. Syst. J. Int. Desulfonatronumaceae and n15 uigtepoeso food of process the during 1956 in Desulfonatronaceae .cooperativum D. 06 6 1–6. 56: 2006, IRBA XRMPIE TTELMT FLIFE OF LIMITS THE AT EXTREMOPHILES MICROBIAL sc,hsbe orce on corrected been has (sic), IJSEM a hw in shown was ) Kee tal. et (Kuever aiainlist Validation : fognssta r bet rwcniuul t6kilorads 6 at continuously grow evolution to h The Gy) able life. (60 are of that never definition organisms was of biological unfortunately any life of radiation in of feature mentioned level this certain and a impossible, without is irradia- Life high growth. require for cer- always levels true below should tion live since but to radiation, exist, of able types fluxes be such tain not that should prove theoretically to radiophiles difficult indeed microorganisms. is radio-resistant It the among radiophiles true are hni h ttoaypaeo rwh(.4kGy). (0.64 growth kGy) of glomerans (0.82 phase stationary phase the (log) in than exponential the 2004). in Lafortune gamma-irradiation and of Lacroix strains 1986; Seven al. et (Hastings ilization (2005). al. et Omelchenko by performed was of research ge- comparative nomic latest The 2000). (Daly degradation compound engineering for approach rans realistic Earlier a sites. showed waste Daly radioactive of bioremediation for organism radiodurans D. essmlrt h yeIIsceinptwy(ic hr is there (since in formation pathway rans pili secretion concerning III data sys- type experimental secretory no the in to involved similar structures tems surface of to formation such contribute the systems, could functions, gene pili-associated entire encoding in genes transferred as role The a (4) play response; may stress repeats The (3) nucleotide bacterium; numerous this of unexpectedly phenotype unusual to the likely in are involved families, be expanded to belong that those desic- particularly the and radiation of extreme resistance the cation both to contribute to likely the are proteins and resistance-associated superfamily desiccation plant hydrolase of homologs Nudix expanded were The conclusions (1) following made: the 2001) al. et (Makarova genome for than 1983). for Evans UV and to (Moseley resistance megarad The 0.8 at they survival and megarad 10% 0.5 show to up irradiation ionizing to response in of die cells phase, damage. growth DNA exponential of the forms In it non-radioactive to and response exposure in temperatures) evolved chronic low resistance to radiation and that high likely more of seems cycles or hydration dessication of and oxi- (cycles environments or non-static light or by (UV agents) organisms agents dizing on physicochemical inflicted common of readily variety is (Makarova a damage years DNA billions 2001). four al. last the et over about rads/year only 20 to provided 0.05 have waters radionuclides, its dissolved including radiation environments, containing the surface Earth’s ago, the years Oklo in billion the levels to two rise (Gabon) gave deposits that a those uranium Notwithstanding like times. reactors radioac- fission geologic highly natural over few of Earth absence on apparent habitats tive the given remarkable, is te aito eitn atrawr on uigfo ster- food during found were bacteria resistant radiation Other o irmdain ea eeito,adtxcorganic toxic and remediation, metal bioremediation, for el) h ocuinatrohrpoemcrsac of research proteomic other after conclusion The cells). .coli E. − 1 a on ob aua otmnn fcarrots of contaminant natural a be to found was rsrieaueirdaindsso ,0 kilorads 1,500 of doses irradiation acute survive or el.Atrcmlt td of study complete After cells. (Mr´ atbclu sakei Lactobacillus .radiodurans D. Deinococcus zk20)sget h plcto fthis of application the suggests 2002) azek .radiodurans D. 2 ait fohrproteins, other of variety A (2) ; and eemr eitn to resistant more were hru thermophilus Thermus .radiodurans D. el s3-odmore 33-fold is cells .radiodurans D. ate ag- Pantoea .radiodu- D. .radiodu- D. onot do 195 R1 Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 twssonta tlwtmeaue (–80 temperatures low at that shown was 1973). al. It gamma et (Anellis Cobalt regimes during temperature different strains at different irradiation of survival the on ments gamma of kGy 5.0 families, irradiation. to and exposure after genera survival known 60% exhibited from and distant very runoffs was spring genetically S˜ hot of from Island isolates the of on study the resis- during radiation described A species 2005). (Sanders thermophilic al. moderately habitats et tant des- spring Albuquerque to 1979; hot Maxcy resistance sampling and per- the by others by were and selected irradiation iccation, were to strains Some exposure formed. without bacteria resistant kGy 0.15 after survived (it bacterium doses). resistant radiation and 196 eln nsria hncmae ogon aum h ex- ( The vacuum vacuum. greater space ground a to to posure caused compared vacuum when survival space in to decline exposure that and ganisms, fepsr oU- aito nld osso ims,such biomass, of losses include radiation UV-B to exposure of levels enhanced significantly of consequences the that concluded H¨ in discussed prehensively after recovery injury. control to radiation targets transport potential as peptide reduction activity, metal and cycle of acid considerations recovery. tricarboxylic include to during respiration, necessary is stress It sys- oxidative was: conclusion enzymic against The reinforce defend that which antioxidants tems, of function the of con- have cells In in accumulated stress. ions oxidative Mn(II) trast, Fe(II)-dependent additional by to leads damage is that cellular proteins, radiation from by Fe(II) death released by cells, caused authors Fe-rich/Mn-poor The for radiation. to that sensitive proposed extremely is and Mn, not but dissimila- for found metal-reducing was tory effect opposite The levels. iron low and manganese intracellular radioresistant high that exceptionally shown accumulate bacteria had bacteria Researchers radio-resistant 2005). of al. et cells (Ghosal inside metals of measurement for magnitude radiodurans of D. orders four and two 10 as use information, to genetic ability the redundant to related The is damage 2000). DNA also desiccation-induced probably al. of and damage et DNA capacity radiation-induced (Billi repair to the cells irradiation that rays hypothesized X authors kGy 15 to ganism Chroococcidiopsis intems eitn irognsswere: faecalis, microorganisms Streptococcus resistant most the tion − nli n i olauspromdeprmna measure- experimental performed colleagues his and Anellis radiation- of isolation the with dealing research Much h feto VBrdaino qai csseswscom- was ecosystems aquatic on radiation UV-B of effect The with performed was work experimental interesting Another te netgtoshv salse htavcu of vacuum a that established have investigations Other cyanobacterium desiccation-tolerant the with Experiments 6 adcesdtesria fdscainrssatmicroor- desiccation-resistant of survival the decreased Pa epciey(afr ta.2002). al. et (Saffary respectively oMge nteAoe;ti pce phylo- species this Azores; the in Miguel ao eosrtdhg eitneo hsmicroor- this of resistance high demonstrated hwnlaoneidensis Shewanella and ∼ 10 laiee faecalis Alcaligenes drsrve (H¨ review ader’s − 6 a erae elsria by survival cell decreased Pa) .radiodurans D. reearadiovictrix Truepera Bacillus .radiodurans D. htacmltsFe accumulates that Chroococcidiopsis ◦ dr20) twas It 2000). ader )drn ioniza- during C) .radiodurans, D. . p DDand PD3D sp. does. .V IUAE AL. ET PIKUTA V. E. might was nltl eetbedfeecsi csse biomass. ecosystem result in and differences fact, common detectable more In little be in production. may primary structure community in in decreases shifts simple not to will limited radiation solar be increased ecosystems to Responses to uncertain. is damage still exposure however is UV-B organisms, aquatic increased to that harmful author, evidence the significant to is According there warming. global of poten- the augmentation in tial sink resulting dioxide, reduced carbon and atmospheric compounds for capacity nitrogen of availability de- in composition, species crease in changes humans, for sources food as eettpso oladetmtd10 estimated dif- and surveyed soil on they of based types later, ferent decade soil A of were kinetics. gram there reassociation per DNA The indicated genomes enormous. (1990) prokaryotic was al. distinct diversity et 4,600 Torsvik their by and published time, paper some for soil in engaged. the are as microbes well these as which structure community in the processes into microbial look to done increasing research be future the can sequences, and rDNA environmental techniques of molecular availability With in expected. appreciated. and advancement once explored be the we to beginning what just is and field This knowledge our exceeding high, Soils in Extremophiles 8. radiation. ionizing to resistant are that strains and species clude and teria), Methylobacterium genera Kocuria, currently The Kineococcus, and species. menobacter, the 2005), 20 al. includes from et genus isolated (Rainey this species Arizona 9 in Desert additional Sonoran an by increased cently hs SC) admapie oyopi N (RAPD), DNA polymorphic amplified random (SSCP), polymor- phism conformation single-strand gel (TGGE), gradient electrophoresis temperature (DGGE), denaturing electrophoresis in- (RISA), gel These gradient analysis available. spacer became intergenic ribosomal also clude samples DNA soil of from amplification al. extracted PCR on et based Tringe techniques 2001; Several Pace 2005). and diversity (DeLong the organisms at uncultured look a of allowed also rRNA 16S targeting sequencing projects Environmental Hofle 1997). 1995; Zhou 1997; Ueda Borneman 1993; 1999; (Stackebrandet analyze soils to in rRNA, population 5S sometimes the and as16S culture- such the A typically subunits operon, of small developed. RNA ribosomal were variety utilized studies that of a number techniques on and methods based independent communities microbial 1997). sess al. et (Bintrim diversity the of 0.1% rep- than only less species traditional, cultivable resented by result, a microbes difficulties As methods. soil the culture-based to characterizing due and only mainly cultivating is has in This however, success. distribution, limited and with effort met composition The the 2002). (Torsvik study soil to pasture in equivalents genome h ubro pce ntegenus the in species of number The irognsswr nw stems bnatspecies abundant most the as known were Microorganisms quite is soils in organisms extremophilic of diversity The nrcn er infiatpors a enmd oas- to made been has progress significant years recent In hroocs Pyrococcus Thermococcus, 10 cell/cm eracaoa)as in- also (euryarchaeotae) Deinococcus cntbce,Hy- Acinetobacter, 3 ihu o8,800 to up with a re- was (eubac- Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 ie ta.(03 nlzdtedvriyo irba genomes microbial of diversity the 2005). analyzed al. (2003) et al. Nagy 2003; et al. Liles et Wery 2005; al. et al. Nemergut et 2003; (Liles world the of parts different from composition, munity indicated whereas 2001). study al. soil, et (Sessitch One particles particle clay in 2000). found large al. in Halophaga/Acidobacterium et dominated (Ranjard Proteobacteria soil of pH. neutral with soils in plateaus (pH soil basic phe- because > extreme, this other whether the know towards to not moves extended nomenon did pH authors as The decrease conditions. richness acidic the and and diversity soil, of neutral com- in level community highest was as diversity well Bacterial as predictor position. geo- richness, best and the on diversity was dependent bacterial soil of of not pH was the and Instead, community diversity, distances. graphic a animal other of and and composition plant latitude, the affect temperature, typically site that di- to variables bacterial unrelated indicated was (2006) versity study vegetation Jackson’s and and ratio, Fierer organic nitrogen type. pH, to size, carbon particle concentration, moisture, carbon soil include: These soil. in Soils in Diversity Microbial 1998). Weller and Raaijmakers 1995; hybridization (Amann for be probes to fluorescent interest the customizing of by groups targeted 2001). specific allows al. also et technique latter (Amann The examination microscopic to direct (FISH) and hybridization perform (Ibekwe situ in membrane fluorescence cell and 1998) of Kennedy profiles (FAME) to Acid Alternatives Ester Fatty include 2000). Methyl examples al. used; been et also have Osborne methods 2000; PCR al. et (Kitts Marsh (T-RFLP) termi- 2001; polymorphism and length 2000) fragment length al. restriction et include nal (Ritchie These (LH-PCR) fragments. PCR detection DNA heterogeneity improve amplified to resolve years recent and in developed have proaches and of capability numbers; amplifying PCR. the low impacting in soil in microbes inhibitors various capturing always soil from not DNA affect samples extracting possibly bacteria; certain methods from lysing recovery DNA cell include: limitations populations. Some certain detecting in introduce biases often in result procedures which The variables, meth- limitations. these without usage, not frequent are and ods popularity their of spite anal- In community ysis. soil in contribution significant made have they 2002; 2006). (Kent Fierer changes biogeographic or dif- treatment the in- to study due the as ferences well enable as compositions methods community these of vestigation from (ARDRA). generated analysis fingerprints restriction The DNA ribosomal amplified and .)smlswr o ayt ban oi suceri diversity if unclear is it so obtain, to easy not were samples 8.5) hr eemn tde hwn atra iest,o com- or diversity, bacterial showing studies many were There size particle the by influenced is diversity Microbial diversity prokaryotic influence factors environmental Many ap- different biases, minimize and circumvent to order In and perform to easy generally are methods PCR-based The eetems omnorganisms common most the were IRBA XRMPIE TTELMT FLIFE OF LIMITS THE AT EXTREMOPHILES MICROBIAL α - ecie hrolaihl sltdfo ui olo hot a of soil humid a from isolated thermoalkaliphile described tem- higher example, Thermophilic with for soils names. in perature; published discovered be recently to from continued organisms few a name to are there and soils; 2003), Then saline 2003). in al. halotolerans residing et organisms (Wery halophilic temperatures low erate Paenibacillus psychrotrophs Brevundimonas, of seobacterium, of number species a example, find Planococcus for to soils; surprising Antarctic not in Kevbrin, Do- is Bacteria and the It Wiegel to main. 2003; belong extremophiles al. these et of Many cambisol Dunfield 2004). forest 2003; acidic al. sediments, et (Wery alkalinic soil, Antarctic extreme; considered i.e. are soil the of conditions environmental the habitats. of acidic variety to a limited only in not found and above, been mentioned have as genus soils this of validated members was 1991, name in its Since 1991). al. et en- (Kishimoto vironment mineral acidic from isolated chemoorganotroph acidophilic iue.Tetp species, Fir- type The and micutes. other Actinobacteria, Proteobacteria, with as compared such inhabitants when soil conditions unusual under growing (Smit organisms uncultured 2001). of al. groups et dominant the showing of one four results, was similar from from field yielded libraries wheat also a clone Holland Furthermore, Arizona. their Northern in in soils bacteria arid identifiable the of (1999) al. et where Dunbar of 2005). those with al. consistent et were findings (Nagy These soils groups agriculture in bacteria major representatives these the low hand, other were of the one On identified. among and was amplified DNA being their in and highest soils, ranked arid clones Desert Acidobacteria-like Sonoran showed Arizona crusts in soil which diversity study prokaryotic Another the springtime. surveyed during and samples winter wet both meadow and in numbers dry summer high in 2005). presented spring, also al. they during and et months; abundant (Nemergut most soil were tundra They alpine Mountains Rocky 2003). al. et (Ochsenreiter detected being ecosys- groups the to and sandy as phyla diversity a similar showed from Germany Darmstadt, obtained near tem being sequences approaches bacterial molecular The the used. on pro- depending Their varied present. portions were delta-Proteobacteria and alpha, gamma of beta, subdivisions all Proteobacteria, the Within Aci- dobacteria. in members to belonged population predominant three-year The a span). within (76–86% groups Verrucomicrobia and Firmi- cutes (CFB), Aci- Proteobacteria, Cytophaga-Flexibacter-Bacteroides the indicated to dobacteria, belonged genes bacteria rDNA the of The majority the Wisconsin. samples Madison, soil in from library collected DNA metagenomic a constructing by te xrmpii raim xse nsi,epcal if especially soil, in existed organisms extremophilic Other cdbcei r osdrdeteohls aal of capable extremophiles, considered are Acidobacteria Colorado the in group predominant the was Acidobacteria Acidobacterium laiatru iburiense Alkalibacterium L ta.2005), al. et (Li swl sohruiutu eea(i.e., genera ubiquitous other as well as rltdognsscmrsdnal half nearly comprised organisms -related neornagottschalkii Anaerobranca cdbceii capsulatum Acidobacteriuim tetmnsoaalba Streptomonospora Nkjm ta.20)just 2005) al. et (Nakajima Psychrobacter htcudtol- could that ) Acidobacterium Marinococcus sarecently a is L tal. et (Li a an was , Chry- 197 and Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 rsn nrc hzshr Gokp ta.19b,patroots plant were 1998b), al. sequences et gene (Großkopf rRNA rhizosphere rice subunit in small present Their plants. with terrestrial in 2003). inhabitants al. the et of (Ochsenreiter component environments unique and of stable a 0.17% constitute crenarchaeota and soil 0.16 Thus, respectively. populations represented the set- sequences agricultural archaeal an and these ecosystem ting, sandy a of rhizosphere soil. the bulk In in 0.5–3% between was abun- from rDNA from relative crenarchaeotal survey of the as dance revealed A Germany well 2003). Darmstadt, in as al. samples et Asia, soil (Ochsenreiter and mats Europe microbial in two di- from areas sampled geographic soils Crenarchaeota different verse the of in lineage present particular consistently This was ubiquitous soil. in were abundant Crenarchaeota and of members nonthermophilic Crenarchaeota. of the composed of is division which planktonic Archaea, the affiliated marine in is the members it of fact, I In Group Archaea. the the with of member cultivated distant any was branch to its but lineage phylum, Crenarchaeota this the indicated within sequences was a clone Phylo- these represent soils. of these to analysis in found genetic communities was microbial organisms the of these component of Wis- cluster Madison, in RNA a collected ribosomal consin, samples soil subunit from small Archaea of the genes cloning 1997). al. and et they amplifying (Bintrim and By realized soil, once in than population widespread more archaeal were an of presence the demon- strated colleagues and Bintrim mi- 1997, traditional In by and methods. studied isolated crobiological and niches, cultivated mostly easily ecological be were not unique could members they or Archaeal environments that extreme fact from mainly the was This to ago. decade due a until recognized not were soils in Soils in Archaea 1995). Ueda 2005; al. Simon et 2004; by Goodman Domain and Archaea (Sliwinski association the they phylogenetic in and phylum Crenarchaeota worldwide, the habitats to belong soil found mesophilic have from studies sed- Several sequences and 2004). soils Kevbrin been neutral and have and (Wiegel mesobiotic iments Alkaliphiles of 2004). variety a al. in from environment isolated et soil (Banat cool Ireland the from Northern isolated were formers spore the be- to them long of most and Tokyo, around areas non- in inhabiting environments bacteria saline halophilic reported (2005) al. et Echigo 2000). al. et cdcfrs absl(ufil ta.20) n w Clostridia two akagii and 2003), Cl. al. et (Dunfield cambisol forest acidic are niches acidic (Sch¨ Park National Yellowstone tepidamonas lus and 2001), Antranikian and (Prowe Kenya in inlet lake 198 utemr,teeceacaoawr on nassociation in found were crenarchaeota these Furthermore, that finding, unexpected this confirmed studies Subsequent Crenarchaeota. places. unexpected in extremophiles some existed there Then Bacillus and Cl ehlclasilvestris Methylocella rgntdfo etemlyhae olin soil heated geothermally a from originated . acidisoli n eae eea opeo thermophilic of couple A genera. related and h rsneadsgicneo Archaea of significance and presence The rmaii etbgsi (Kuhner soil peat-bog acidic from fe ta.20) xmlsin Examples 2004). al. et affer ehntohfo an from methanotroph a , Geobacil- .V IUAE AL. ET PIKUTA V. E. fceacaoe ilhpflyapa ntena future. near the in appear hopefully will novel crenarchaeotes culture As axenic of 2005). the developed, al. be to et continue (Simon methods cultivation unknown still were growth their supporting substrates actual the although enrichment extract to root positively crenar- responded mesophilic organisms sur- These culturing reported. to of was evidence chaeotes began first progress the Some as lately, identified. face and member isolated no and been methods has culture-independent by stud- done the all were recently, ies Until significant. is asso- roots their plant and with 1997) ciation al. et (Bintrim role ecological important an pH and and microcosms, amendments sources increases. soil nitrogen by these affected not in were they stable very archaeal were The sheep. communities grazing from their largely where were sources grassland) from nitrogen native those (i.e., than pastures community upland crenarchaeal unmanaged different a had fertilizer input nitrogen inorganic with pastures Managed (2004). al. et 2004). Goodman and (Sliwinski environmental factors by and mediated was plant relationship their between and microbes, interactions na- the authors in reflected plants the environments with Therefore, tive associations lineage. crenarchaeal plant the that on concluded dependent and soil, not bulk was to compared it the as from rhizosphere result in to richness seemed increased difference cor- This in soil. obtained pro- bulk those the from responding distinct showed were They rhizosphere Wisconsin. from in files bulk locations in different present at those soil with rhizosphere the inhabiting consortia crenarchaeal the compare to (PCR-SSCP) polymorphism mation ecology. devel- and root for opment implications important had organisms these roots, thus, senescent of colonizers good particularly were they fact, frequency.In high both unexpected an colonized at roots Crenarchaeota plant senescent soil and young showed sequences, (2000) culture- gene al. rRNA and et subunit Simon microscope small of epifluorescence recovery Using independent (Bomberg 2003). Simon seeding pine al. 2001; of Triplett et mycorrhizospheres and and (Chelius 2005), al. tomato et and maize as such isweeteeognsseita n ftemjrbiogenic major the of one as pad- exist rice organisms flooded these from where especially dies soil, field paddy in done were anaerobic obligate their of spite species (Euz´ in characteristics and since, genera described Many been Domain. have Archaea the the in to recognized members earliest related the among were were methanogens not since sequences was surprising, finding the This phylum. of Euryarchaeota the Most in methanogens US. Okefenokee subtropical the the in to bogs swamp Siberia West cold surveyed the (2003) from ranging wetlands, al. distinct using geographically et from By samples Utsumi soil Crenarchaeota. peat amplification, to PCR addition rRNA in 16S soil of types different Euryarchaeota. play crenarchaeotes soil mesophilic indicate results these All Nicol by shown as pastures upland in reside also Archaea confor- stranded PCR-single used Goodman and Sliwinski oto h rhelcmuiysuiso Euryarchaeota on studies community archaeal the of Most b 2006). eby te rheldvriyhsbe on in found been has diversity archaeal Other Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 .AtoilgclSgicneo Extremophilic of Significance Astrobiological 9. roles. ecological be their to elucidate and waiting study phylum to order Euryarchaeota in the discovered Obviously in 1998b). members al. are et there cluster (Großkopf any to rice groups affiliation other any euryarchaeal without The other decent of relationship. line distant main novel a a had formed the only on it grouped but clusters II, rice the as of branch branch- One same phylogenetic noted. a was not pattern only were ing and cultures lineages Pure microcosms, these soil. rice paddy from flooded rice available Italian of of roots slurries rice in soil, and bulk detected anoxic been the (2000) have that addi- al. in lineages et In archaeal Liesack 2000). novel species, several al. noticed methanogenic et known Ramakrishnan the to 1999; al. tion et al. Großkopf et 2000; al. Chin et 1998a; (Liesack size tempera- particles concentration, soil and acetate ture, di- by as These influenced such 1997). were factors al. organisms environmental et methanogenic Min of 1998a; patterns al. verse et Großkopf 2000; (Liesack al. methanogens et hydrogenotrophic in found group major Methanobac- (species the family of teriaceae members whereas methanogens; utilizing (species taceae slwa –20 as low temperatures as at activity very metabolic maintain that for can and organisms (lyophilization) viable some freeze-dried when remaining that time known of of well periods is capable long It generally 2005a). ice al. are in et microbes Pikuta cryopreserved 2004; when al. time et of (Abyzov periods geological for worlds. able frozen are astrobiol- System Solar to our interest of bodies major most of since ogy, is temperatures subzero and/or Italian indicate on to Reports seem 1998a). soils al. naceae paddy et rice (Großkopf Japanese Italy and in soil dry enfudt ecpbeo elcto n rwha –5 at growth and replication of capable be to found been ffloe iemcoom;i at ewe 10 between fact, soil in bulk microcosms; anoxic the rice periods. in flooded oxic found of and are dry methanogens the of majority during The survive can they and genesis, c xsstdyi atdpsta h ot oa c a of Cap Ice Polar North the at deposit vast water that a established Pikuta in well today and now exists Hoover is ice It 2002; 2006). al. al. moons et et icy Abyzov of (Hoover 2004; crusts Saturn ice and the nuclei and Jupiter the water per- of of liquid the surface the in the in or near found comets, Mars, be of of might caps ice that polar forms or life mafrost for analogs best the 2006a). al. et (Pikuta conditions anaerobic and aerobic both fH of raim tlz H These utilize 2000). al. organisms et (Liesack flooding most by the caused to the condition due anoxic environments are these in Methanogens archaea important methane. functionally atmospheric of sources Microorganisms thsas ensonta irognsscnrmi vi- remain can microorganisms that shown been also has It low at microorganisms active metabolically of study The h irflr ftecyshr fpae at provides Earth planet of cryosphere the of microflora The 2 -CO ie,species (i.e., 2 tlzn ehngn eedtce e rmof gram per detected were methanogens utilizing ◦ .Rpeettvso h genus the of Representatives C. hrolsaacidophilum Thermoplasma M . 2 -CO concilii .brei .mazei M. barkeri, M. 2 .bryantii M. raeaea usrtsfrmethano- for substrates as acetate or eetepeoiatacetate- predominant the were ) , .formicicum M. IRBA XRMPIE TTELMT FLIFE OF LIMITS THE AT EXTREMOPHILES MICROBIAL n Methanosae- and ) Trichococcus n aiegroup marine and 6 Methansarci- o10 to eethe were ) 7 ◦ have cells Cat eaue ntesraeo aswr esrdb ahne to 20 Pathfinder by exceed measured sometimes were Mars tem- of atmospheric surface the daytime on to Earth peratures The on comparable 2003). soil is Dickson forest which and rain tropical (Odokuma mass of by (13–19%) water content water having of the N) 16% 10 E, over (30 region with moistest soil the with in soil 2004) of al. layer et lower Fos- (Mitrofanov the water Medusae 9–10% and hemispheres. exhibited Terra even both (Arabia sae) equator in the degrees near 60 regions than Two greater exceed to latitudes found was at regolith 11% Mars of the layer of cm) content (10–20 surface, water thicker The a the soil. by covered near are they very south are the in permafrost but of latitudes, layers northern water-ice the In these Mars. of regions the polar both South at fraction, and mass permafrost North by water-rich water 50% large to up are contents there with areas, that al. found et (Litvak also spacecraft has Neu- Odyssey 2006) Energy Mars High the aboard The detector 2001). water-icetron al. seasonal et (Paepe the cycles with freeze-thaw associated expansion effects by contraction produced double-rimmed are and that the Earth with of permafrost consistent in are polygons that Mars double-rimmed on of images polygons produced had Surveyor The 2000; 1990). Global Jakosky al. Mars and et Haberle Bass 2000; Greve 2000; 1976; Paige al. and et Kieffer Bass 1998; al. et (Zuber Mars n eu,adrcn ocncatvt nI a enre- been has Io on activity volcanic the by tec- recent vealed or Mars and on volcanic Venus, activity have volcanic and that ancient system for Evidence solar activities. may our tonic as of such bodies systems on thermal exist acidic with concerned primarily research. Astrobiology for targets Europa, prime Mars, other on life and present or past for of search evidence to and needed and biomarkers be design will the that to systems importance robotic great of of development cold- is the planet in our thrive of that regions microflora est Earth’s of The species microorganisms. the of that eukaryotic study communities and microbial prokaryotic of both growth include the provide for that conditions minerals and ideal chemicals, organic results gasses, water, glaciers uid in liq- trapped entrained with 2004b; ecosystems) rocks (cryoconite Hoover microenvironments albedo in low and of Pikuta Earth, heating On 2004). solar 2002; al. et al. Mancinelli 2001; Gilichinsky et and Hoover (Hoover glaciers (halophiles) channels in Microorganisms brine and (cryptoendoliths). (acidophiles) acidic regions inhabit also polar frozen in the and permafrost of in water rocks of films thin microorgan- within Many lakes. grow or isms seas as liq- such in bodies, found large be in water state the uid that necessary not clearly requirement is universal it the water, is for Earth on known life com- all one for the bond that mon accepted generally is it and While ice Astrobiology. significance water to great of the is in regolith Martian state) modern the cryopreserved in a permafrost in present be (or day 1998). Levin and (Levin Mars for on suitable life conditions interstices current provide the could between This ice grains. surface permafrost near of of melting to due water h motneo tdigaiohlcmcoraim is microorganisms acidophilic studying of importance The to- thrive might extremophiles microbial that possibility The iig ahne,Goa uvyr asOdyssey, Mars Surveyor, Pathfinder, Global Viking, ◦ htcudyeddunlfim fliquid of films diurnal yield could that C 199 Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 ieto.Hwvri smc lsrt h u n thsasur- a opposite has it the and 470 in around Sun of rotates the temperature to it face thought closer although much is Earth is Venus it of However System. planet direction. Solar twin as the a known as of is of planet which Venus, acidic vol- on most Much occurred the 2004b). also Hoover has and activity and gamma-ray, canic (Pikuta IR, data and spectral images neutron radar and infrared, traviolet, Venera,Voyager, 200 ocis oeie nclne iheeto rnprn car- irregular transparent and electron spherical with as colonies Cyanobac- in occur the sometimes forms of coccoids, the orders of five associations Some all clear teriaceae. of provide morphotypes that known features with exhibit nanostruc- they ALH84001 and the than tures complex more and are larger forms These much 2006). carbona- Hoover (CM2) 2005; (Hoover Murchison meteorites and ceous (CI1) Orgueil the in mats terial cyanobac- and microorganisms filamentous and coccoidal di- of verse assemblage complex and large a of remains mineralized the System. Solar environments the hostile in most elsewhere Earth’s best and in to life how of and evidence where for delineate search to and to biomarkers helped valid have define results ALH84001 re- the extensive by triggered bacterial The efforts search meteorites, extremophiles. of microbial study and re- paleontology, the these stimulated microfossils, profoundly recognized be sults valid to as as size accepted sufficient certainly of not the were though Even nano-structures 2003a). ALH84001 al. Earth et on (Pikuta systems previously carbonate discussed of was formation in agents microbial participation of The Mars. on evidence minerals carbonate definitive of provided existence the meteorite of this of study The the 1996). Lugmair in and Wadhwa 1996; microfossils al. et putative (McKay meteorite the ALH84001 with association biogenic in possibly with magnetites rimmed globules car- abundant carbonate of and findings bonates the by enhanced was Astrobiology for sheet. ice inter- the at and niches water liquid in the thrive between could faces psychrophiles Hoover and that (Pikuta and Europa 2004a), in- on vents also hydrothermal It might acidic moon. microorganisms habit icy acidophilic this that of crust conceivable the is underneath ocean for water necessary liquid heat the the provide effects could tidal vents Jovian hydrothermal The exists. and/or crust ocean ice water liquid fractured the the Europa, beneath of that evidence much also is There lithotrophs. sulfur-metabolizing acidophilic of development for the suitable springs and geysers acidic provide also could activity the volcanic for Io’s microorganisms. acceptable sulfur-dependent be of may development that conditions with System Solar our has atmosphere Venus the discussed. of been clouds dense acidic on cooler forms the life in of droplets existence possible about view stratosphere) in of of point (level microorganisms the km active 44 of of altitude an 2002) at atmosphere al. Earth’s After et atmosphere. Earth’s (Harris of discovery that the times 100 to equivalent is that eetsuishv eutdi h eeto feiec for evidence of detection the in resulted have studies Recent microorganisms alkaliphilic of study the of importance The of body volcanic active most the presents Io moon Jovian The and Magellan ◦ pc isoswt pia,ul- optical, with missions space ,ada topei pressure atmospheric an and C, .V IUAE AL. ET PIKUTA V. E. .Smlsfo aoakln csses-oalksin lakes ecosystems—-soda halo-alkaline from Samples 3. near Springs Hot ecosystems—Chena acidic from Samples 2. Pleistocene planet—frozen our of regions cold from Samples 1. the of included: These number Earth. a on environments to extreme the expeditions most in field of during out variety a collected carried evidence used samples Research for has Cosmos. search Laboratory the Astrobiology to NASA/NSSTC in how elsewhere and life where of understand us help order to in Astrobiology of field emerging rapidly the in importance Research Astrobiology Solar for Investigated Extremophiles Microbial the in 1986). cells al. et living Hoover 1981; of Wickramasinghe and distributors (Hoyle System and carriers meteorites be and comets could that 1981 in Wickramasinghe and by Hoyle proposed hypothesis the supports 2007) meteorites carbonaceous (Hoover in microfossils of indige- detection as The interpreted microfossils. been nous have forms biologi- the recent and to contaminants attributed cal be cannot that they ratios that C/S establish and clearly C/N, C/O, anomalous have has they Analysis that revealed X-ray Dispersive other and Energy minerals microstructures. with abiotic confused be biogenic cannot distinctive that and characteristics complex These extremely Stigonomatales. have and microfossils Nostocales mor- Orders: representing the as of interpreted photypes exceptionally are are that filaments forms Orgueil well-preserved the of distinctive most The morphotypes genera the of of members characteristic of features detailed with akinetes) ellipsoidal exhibiting sub- (occasionally the heterocysts to basal attached by stratum tapered forms benthic the represent of to Many appear filaments cells. differentiated highly and false branching and true constrictions, cross-wall polar- exhibit tapered and have been filaments that ized forms also other of number has a contain meteorite to found Orgueil the Oscillatorianlean However, the of cyanobacteria. sheaths, filaments of carbon-rich trichomes and the mineralized size and with both frac- in features freshly consistent morphological are in detailed meteorites found the forms The of surfaces filamentous matrix. tured rock the meteorite of the majority in vast and that embedded uniseriate mats found as and been filaments occur have branched that and forms unbranched larger multiseriate the as distinctive not so with are forms simple consistent morphologically These forms Pleurocapsales. the baeocyte-like are with Others pseudo-filaments Chroococcales. in the of mor- characteristics as with interpreted photypes are and envelopes mucilaginous bonaceous ti elkonta irba xrmpie r fgreat of are extremophiles microbial that known well is It California; Alaska; Fairbanks, Vostok and Mountains, Thiel Hills, Antarctica; Station, Patriot ice deep the and from rocks, snow, cores and penguins Chile; Magellanic Patagonia, the southern of of guano lowlands Kolyma Siberia; the Northeastern of of permafrost Alaska; of Glaciers and Tunnel Fox of permafrost and wedges, ice ponds, thermokarst Calothrix , Rivularia and , Tolypothrix . Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 scretyi preparation. in currently is biaeyaiohlcsri AGC2 strain acidophilic obligately 4. tani bet rwo h eimwt ihcnetain of concentrations high with medium Fe the on grow to able is strain spore-forming mesophilic, This 2004a). Hoover and (Pikuta ture 5. 2. 3. .Smlsfo esr n oeaetemlsprings— thermal moderate and geysers from Samples 5. Deep vents—Rainbow hydrothermal deep-sea from Samples 4. 1. Mi- International Collections: in Culture deposited crobial and them published of validly Four California. been in have Lake sys- Mono halo-alkaline and Lake from Owens described of were tems and bacteria cultures mesophilic pure in alklaliphilic isolated of strains Five studied. 2 rmteaii ytmo hn o pigi lsathe Alaska in Spring Hot Chena of system acidic the From h olwn ruso irognsswr sltdand isolated were microorganisms of groups following The itn tfo te nw relvn spirochetes. free-living known differen- other features from physiological it of tiating number a Owens has from it and culture Lake, enrichment was cellulolytic strain a alkaliphilic from and isolated anaerobic obligately this cation; neoigl multivorans Anaerovirgula acids; amino on of reaction pairs Stickland certain a performing by respiration is of strain This al- capable Lake; anaerobic Mono in of per- community anaerobe microbial secondary species kaliphilic a This of 2003d); function al. the et forms and (Pikuta products acids organic proteolysis some of decomposition for responsible Spirochaeta al. et (Pikuta lineage species 2006b); separate separate and level a from genus taken separate distant the had on phylogenetically and be species to clostridial known acids. found organic was degradation some strain is and This species molecules this products proteolysis weak. for very of function as trophic process major this showed The study sequent but Owens Lake, of community microbial anaerobic the in agent lolytic eufntou thiodismutans the Desulfonatronum of strategy the for economy; biotechnol- fuel Hydrogen alternative for an potential as applications offers ogy that product major a metabolic as end hydrogen molecular this of of production feature is peculiar strain the unique continent; American the on spiro- chete sugarlytic free-living alkaliphilic and anaerobic ligate idli californiensis Tindallia molecules; rwecuieyo yrgnadCO and hydrogen on exclusively grow to has bacterium this it allows that that is metabolism strains chemolithotrophic Asian a feature from specific it a differentiating strain as this and of continent, American bacterial the sulfate-reducing on alkaliphilic species obligately first the be lsaadCalifornia. and Alaska Atlantic; Middle Azores, Vent, Sea prcat americana Spirochaeta + ihp .–..Tetxnmcdsrpino hsstrain this of description taxonomic The 1.5–2.0. pH with p ASpC2 sp. ASpG1 T APO snwi rprto o publi- for preparation in now is SCA T T a ecie sa agent an as described was T a on ob h rtob- first the be to found was T FML1 a sltdi uecul- pure in isolated was a on stecellu- the as found was IRBA XRMPIE TTELMT FLIFE OF LIMITS THE AT EXTREMOPHILES MICROBIAL 2 T ihu n organic any without a lofudto found also was euigacabceilsri OGL-20P strain archaebacterial reducing htgosa eprtr ihrta 120 than higher temperature a at grows that pce facaaaogtehprhrohlsis hyperthermophiles the alkaliphilus, among coccus archaea of species h rtoyi scrtlrn atru tanPPP2 of strain description bacterium The psychrotolerant 2006a). proteolytic al. the et (Pikuta for culture temperature pure known a lowest of growth the is record This conditions. bic un,adi a bet rwat grow to able was it and guano, psychrotolerant of species 2007). new al. et separate (Pikuta a to genus belongs the isolate This described. hr eido iea 130 at time of period short yaseiso rhe.Tems hrotbeseisis species 120 thermostable most The fumarii archaea. rolobus of species “populated” extensively a most is by and busy The quite is Earth. acidophiles species cooling of thermophilic hot, moderately and a hyperthermophilic on of acidophiles area of origin concerning view primary de- of the point and our for found evidence been provides that have see, scribed; can species we psychrophilic As acidophilic shown. is no species trophic square acidophilic this of of of distribution side balance the left the the On ecosystems. for surrounding in responsible chains microbial agents described and environmen- important known and tally pH of pathogens, saprophytes, majority neutral includes a that of species of repre- area region an square the sents in this square limits; painted mesophiles/moderate-thermophiles gray 1a) a (Figure pH/temperature shows known diagram The follows. described as be pic- will of the ture matrix, corresponding names the on microorganisms the of radia- species placing salinity/pH, by salinity/temperature, tion/temperature pH/temperature, of CONCLUSION AND INTERPRETATION penguin). Magellanic preparation the in from also guano also is is species isolation of and (source genus new separate a resents hccu patagoniensis chococcus ssfo h c n emfotsmlso te oiso the of bodies other of System. samples Solar permafrost and microorgan- ice living the revive from to isms possible is cryobiology it to that important demonstrating also by cryopre- is was It permafrost. it ancient and in period served validly Pleistocene impor- a the first great of is species of It published Paleontology. is and bacterium Astrobiology both This phenotypic to 2005a). tance and al. genetic et on (Pikuta was both levels it species since known species new from separate different a as described was fermenting bacterium anaerobic facultatively This Tunnel Alaska. Permafrost Fairbanks, Fox near CRREL Pleistocene the of the pond in Thermokarst a years of 32,000 ice for frozen remaining after alive rmade-e yrtemlvn h biaeysulfur- obligately the vent hydrothermal deep-sea a From h td fsmlsfo odrgosldt icvr of discovery to led regions cold from samples of study The fw osdrtedsrbto flf namatrix a in life of distribution the consider we If nte neetn scrtlrn ualtcbacterium sugarlytic psychrotolerant interesting Another ◦ ,adtenurpii u o ail ulse tan121 strain published validly not but neutrophilic the and C, Thermococcus htcudsrie3–0mni natcaeat autoclave an in min 30–60 survive could that anbceimpleistocenium Carnobacterium hc sal ogo tp 05 nthe On 10.5. pH at grow to able is which PmagG1 ihpooe name proposed with ◦ .Tems laioeatdescribed alkalitolerant most The C. − T 5 a sltdfo penguin from isolated was ◦ tarbcadanaero- and aerobic at C ◦ T n uvvsfra for survives and C a sltdand isolated was FTR1 .thioreducens T. T T Thermo- htrep- that htwas that Tri- 201 Py- Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 202 bet rwa H1. n t te pcfi etr steabil- the is feature at specific grow other its to and ity 10.0 pH at grow to able de- species recently psychrotolerant The organisms. scribed living all among leaders alkalitolerancy the in are cyanobacteria mesophilic was previously, As discussed archae-bacteria. and cyanobacteria, shown; bacteria, is and includes mesophilic microorganisms it of of distribution species the thermophilic square moderately gray the of side right I.1. FIG. hts ahgn,adevrnetlaet) sw a see, can we As agents). (sapro- environmental microorganisms and of the species pathogens, represents known phytes, square of painted majority gray a the of area side the left On the matrix. on this diagram within microorganisms of species known of for established bacteria. was sulfate-reducing temperatures of species subzero psychrophilic at growth of record Koluhe l 99;()Slnt,%(/)p;()Slnt,%(w/v)/Temperature, % Salinity, (c) (w/v)/pH; % Salinity, (b) 1999); al. et (Knoblauch h iga fslnt/H(iue1)sostedistribution the shows 1b) (Figure salinity/pH of diagram The itiuino nw pce fmcoraim ntemti:()pH/Temperature, (a) matrix: the in microorganisms of species known of Distribution − 5 ◦ .Bfr h icvr fti pce the species this of discovery the Before C. c (d) (b) (c) (a) rcoocspatagoniensis Trichococcus .V IUAE AL. ET PIKUTA V. E. is fhlpiydrn h vlto flf.Teacmlto and accumulation Na The of life. diagram, solubility of appearance evolution This the later salinity. during the 15% halophily about of by hypothesis limited the confirms and again, area once 12 spread pH are Cyanobacteria the salinity. (w/v) to 30% at grow to able are genera the 5%. before of salinity of Species regions in appear acidophiles extreme the rmriloenwsntslya all. at salty not was working: the ocean is hyperthermophiles; primordial non-halophilic Earth were on organisms evolution salin- first of extreme the rule at the known again, Probably, are None ity. species (25–30%); hyperthermophilic area saline the extreme of an species in thermophilic microorganisms moderately of and mesophilic a of presence evolution. Earth’s of stages latest the in ◦ h iga fslnt/eprtr Fgr c hw the shows 1c) (Figure salinity/temperature of diagram The ;()Rdain kGy/Temperature, Radiation, (d) C; ◦ C; ∗ + R-5gnr fpyhohlcslaerdcn bacteria sulfate-reducing psychrophilic of genera 5 SRB- n Cl and Natronobacterium − osi ae eaepsil only possible became water in ions ◦ C. and Natronorubrum Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 ohls aohlchprhrohls ao ralkaliphilic or halo- hyperthermophiles, barophilic mophiles, ther- halo-alkaliphilic thermophiles, observe we acidophilic now of that existence environ- fact the the aggressive by supported ob- multiple organisms is This developed the formed factors. mental even to newly or (phily) result, tolerant, requirement a ligate resistant, As were time. that same appeared the cells at fac- biological physico-chemical evolution, tors extreme of several process experienced have the could During well. not as vec- included forward tors and It back probably, character. but influence, complicated multi-factor changes only a new the had to environments response in of cells ancestor in occur to tations surface? a to (initial light) center of absence the and from pressure opposite, high it or of Was requirement center, of Cosmos? to delivery the surface the in the or sources from Earth exogenous on from life life of microbial distributed origin life endogenous is the How after arises: Another biology microorgan- ecosystems. in among question deep-underground fundamental formed and deep-sea was macroscopic with of barophily life isms the as of them still forms on but organized influence highly sizes, cells, the significant archaean for a and has have bacterial it not of does sizes tiny pressure the the masses to land Due the Earth. on dominated of climate arid the when stage latest the as developed perhaps Halophily possible. became alkaliphily nuhbfe ocnrto fCO of and concentration precipitation buffer mineral enough certain after only and Earth, biological on the history in phase initial the this was pri- and probably been Acidophily excluded, have mary. would is metabolisms of planet types the anaerobic that of means cooling and oxygen formation Free the surface. a at planet after the on developed drop have temperature to significant have of would role Psychrophily the ancestors. as the priority obvious, have is re- microorganisms it planet then hyperthermophilic any regime of high-temperature formation certain the a If microbial quired today? extremophilic observe the diverse we was that whole who world the So, from life? ancestor day in- first present that into cultures developed cell and of teracted there types were different or Earth, physiologically on several homogenous evolution of biological source started single culture appropri- exclusively cell an it that Is suggest evolution? had to Earth’s ate cells the to during etc.) experienced forms, been trans- inactive mutations, metabolically (adaptation, into formation changes biological of very direction been not has have extremophily to of Science area investigated. for thoroughly this need since great data a more very is these resolve there to comets questions order by In important Earth? transported Early were the to and meteorites high and ra- very where were cosmos levels these the diation that in possible elsewhere on it is irradiation originated Or microorganisms of number? level this around irra- the was that kGy Earth Early suggest 30 that tolerate Does could species level. archaebacterium) diation Three an radiation/temperature. them of of (one matrix the in species h euneaddrcino uain htalwdadap- allowed that mutations of direction and sequence The okn tteedarm h oia usinrie:What raises: question logical the diagrams these at Looking known of distribution the shows 1d) (Figure diagram final The 2 ntearteocrec of occurrence the air the in IRBA XRMPIE TTELMT FLIFE OF LIMITS THE AT EXTREMOPHILES MICROBIAL opeeo otsse,poetv ufc oa n animals and (rhi- flora) plants surface both protective for system, true root equally of is zosphere ex- it cannot prokaryotes; organisms without eukaryotic that ist established well ex- now the is role. again It pioneering a process, played this remains probably In microorganisms still biology. tremophilic it in and Earth, problem on unsolved plants an of distribution mo- the key for the was ment formation (mostly Soil agents biological minerals. of the and interaction microorganisms) of the face of important product modern a extremophiles the is of Earth Indeed, sciences. study fundamental the many history, makes to environmental feature memorized this that and genome have because do relics, called they appropriately mod- be all could be reason, extremophiles this can ern For deposits. this rock forever, and others mineral on by observed replaced physi- the completely unique were and with ology changes populations climatic some processes global geo-formation the pure such After to in activity. just or minerals metabolic processes bioleaching and the to rocks due of occurred regions formation the extremophilic certain and of populations, explosion demographic ex- had the regions spe- perienced wide-spread under or evolution local of where all periods circumstances, certain etc., cific in pyrites, formed car- iron were Fossilized gold, them activity. methane, of sulfur, biological elemental of oil, result bon, the is indirect fossils or and minerals of direct of chronology formation The encoded geo- activity. an biological All ecosystems. represent con- balanced deposits species of paleontological creation biological the other to and led sequently environment the with isms relationships environments. extreme such in that developed been possible also quite have initially is related vitamins) It by cultures. exchange microbial an or compounds (un- symbiotically trace two detected of when cells (cases separate cultures cannot microbial microbiologists binary the as in phenomenon also such and efficiency, energetic (mi- for organisms chloroplasts) eukaryotic and of tochondria levels genetic on and reflected cytological are the organisms microbial of kinds different relations between Symbiotic physiologically communities. and then led and functionally that consortia, adjusted microbial the species, of these surrounding creation of of the all to neighborhood products, the metabolic limit end trivial quite poisons, by antibiotics, inhibition of an excretion or an ex- phys- as is and such behavior this specifics specific level iological the interspecies effectively: the more On even out. and pressed die predominant, and forms strongest weaker eat the the that are better, those breath cells: and between more relations competitive has always as another designated cells, and ical developed living was affecting factor ecosystems important very the of environmen- the influence for Except tal levels. cataclysms geophysical global any and at climatic any extinct on In become changes. easily stressful would life future case, the the towards in neces- pool” effects a “buffer providing environmental for sary of flexibility enough map have probably the and as past read microorgan- be extremophilic could of isms genetics The etc. psychrophiles, o h neato fgoigadacmltn organ- accumulating and growing of interaction the So, ieisl vno h ee fmntpco ueculture pure or monotypic of level the on even itself Life . biolog- 203 Downloaded By: [University of Alabama at Birmingham] At: 16:09 17 July 2007 mn,JP,adTse .20.Epnigfotesi epsbufc micro- subsurface deep in frontiers Expanding 2005. 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